Abstract
Heat shock proteins (HSP) play an important role in cellular homeostasis; however, they have recently been involved also in diverse relevant biological processes, like cellular proliferation and differentiation. It has been suggested that they could play an important role in some pathologies, such as cancer and atherosclerosis, making them an attractive therapeutic target. The high degree of HSP’ conservation along evolution suggests that these proteins provide intrinsic defense mechanisms to cells against stress conditions. This chapter provides general information on heat shock proteins, as well as on their role in some pathophysiological processes related to reproduction. It also approaches the association of HSP with hormones and their participation in steroidogenesis, because hormones are critical mediators in regulating development, reproduction, and homeostasis in general. This chapter emphasizes the Hsp60, which has been suggested to have a relevant role in steroid hormones synthesis; besides, this protein is located in mitochondrial contact sites favoring progesterone synthesis in the human placenta.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- 3β-HSD:
-
3 beta hydroxy steroid dehydrogenase
- ACTH:
-
adrenocorticotropic hormone
- AKT:
-
protein kinase B (PKB, Akt)
- APAF-1:
-
apoptotic protease activating factor 1
- APG-1 protein:
-
ATP and peptide-binding protein in germ cells
- BAD:
-
Bcl2-associated agonist of cell death (Bcl2-L-8)
- Bax:
-
apoptosis regulator (Bcl2-L-4)
- ERK:
-
extracellular signal-regulated kinases
- FSH:
-
follicle-stimulating hormone
- HDL:
-
high-density lipoproteins
- HspB1:
-
heat shock protein beta-1
- LH:
-
luteinizing hormone
- LPS:
-
lipopolysaccharide
- MLN64:
-
metastatic lymph node 64 protein (STARD3)
- P450scc:
-
cholesterol side-chain cleavage enzyme
- PI3K:
-
phosphoinositide 3-kinase
- PKA:
-
protein kinase A
- RAF kinase:
-
rapidly accelerated fibrosarcoma kinase
- SMAC:
-
second mitochondria-derived activator of caspases
- StAR:
-
steroidogenic acute protein (STARD1)
- TIM:
-
translocase of the inner membrane
- TNF:
-
tumor necrosis factor
- TOM:
-
translocase of the outer membrane
- TSPO:
-
translocator protein
- VDAC:
-
voltage-dependent anion channel
References
Alard JE, Dueymes M, Youinou P, Jamin C (2007) Modulation of endothelial cell damages by anti-Hsp60 autoantibodies in systemic autoimmune diseases. Autoimmun Rev 6:438–443
Alard JE, Hillion S, Guillevin L, Saraux A, Pers J-O, Youinou P, Jamin C (2011) Autoantibodies to endothelial cell surface ATP synthase, the endogenous receptor for Hsp60, might play a pathogenic role in vasculatides. PLoS One 6:e14654
Arya R, Mallik M, Lakhotia SC (2007) Heat shock genes – integrating cell survival and death. J Biosci 32:595–610
Bahat A, Perlberg S, Melamed-Book N, Lauria I, Langer T, Orly J (2014) StAR enhances transcription of genes encoding the mitochondrial proteases involved in its own degradation. Mol Endocrinol 28:208–224
Becker B, Multhoff G, Farkas B, Wild PJ, Landthaler M, Stolz W, Vogt T (2004) Induction of Hsp90 protein expression in malignant melanomas and melanoma metastases. Exp Dermatol 13:27–32
Belhia F, Gremlich S, Muller-Brochut AC, Damnon F, Hohlfeld P, Witkin SS, Gerber S (2010) Anti-60-kDa heat shock protein antibodies in fetal serum: a biomarker for unexplained small for gestational age fetuses. Gynecol Obstet Investig 70:299–305
Bocharov AV, Vishnyakova TG, Baranova IN, Remaley AT, Patterson AP, Eggerman TL (2000) Heat shock protein 60 is a high-affinity high-density lipoprotein binding protein. Biochem Biophys Res Commun 277:228–235
Boncoraglio A, Minoia M, Carra S (2012) The family of mammalian small heat shock proteins (HSPBs): implications in protein deposit diseases and motor neuropathies. Int J Biochem Cell Biol 44:1657–1669
Burdon RH, Slater A, McMahon M, Cato AC (1982) Hyperthermia and the heat-shock proteins of HeLa cells. Br J Cancer 45:953–963
Campanella C, Bucchieri F, Merendino AM, Fucarino A, Burgio G, Corona DF, Barbieri G, David S, Farina F, Zummo G, de Macario EC, Macario AJ, Cappello F (2012) The odyssey of Hsp60 from tumor cells to other destinations includes plasma membrane-associated stages and Golgi and exosomal protein-trafficking modalities. PLoS One 7:e42008
Campbell AM, Chan SH (2008) Mitochondrial membrane cholesterol, the voltaje dependent anion channel (VDAC), and the Warburg effect. J Bioenerg Biomembr 40:193–197
Cehovin A, Coates AR, Hu Y, Riffo-Vasquez Y, Tormay P, Botanch C, Altare F, Henderson B (2010) Comparison of the moonlighting actions of the two highly homologous chaperonin 60 proteins of Mycobacterium tuberculosis. Infect Immunol 78:3196–3206
Chandra D, Choy G, Tang DG (2007) Cytosolic accumulation of HSP60 during apoptosis with or without apparent mitochondrial release: evidence that its pro-apoptotic or pro-survival functions involve differential interactions with caspase-3. J Biol Chem 282:31289–31301
Chen S, Bawa D, Besshoh S, Gurd JW, Brown IR (2005) Association of heat shock proteins and neuronal membrane components with lipid rafts from the rat brain. J Neurosci Res 81:522–529
Chen C, Zabad S, Liu H, Wang W, Jeffery C (2018) MoonProt 2.0: an expansion and update of the moonlighting proteins database. Nucleic Acids Res 46:D640–D644
Cheng Q, Chang JT, Geradts J, Neckers LM, Haystead T, Spector NL, Lyerly HK (2012) Amplification and high-level expression of heat shock protein 90 marks aggressive phenotypes of human epidermal growth factor receptor 2 negative breast cancer. Breast Cancer Res 14:R62
Chun JN, Choi B, Lee KW, Lee DJ, Kang DH, Lee JY, Song IS, Kim HI, Lee SH, Kim HS, Lee NK, Lee SY, Lee SY, Lee KJ, Kim J, Kang SW (2010) Cytosolic Hsp60 is involved in the NF-kappaB-dependent survival of cancer cells via IKK regulation. PLoS One 5:e9422
Cuffe JSM, Holland O, Salomon C, Rice GE, Perkins AV (2017) Review: placental derived biomarkers of pregnancy disorders. Placenta 54:104–110
Czarnecka AM, Campanella C, Zummo G, Capello F (2006) Mitochondrial chaperones in cancer: from molecular biology to clinical diagnostics. Cancer Biol Ther 5:714–720
de Graaf R, Kloppenburg G, Kitslaar PJ, Bruggeman CA, Sassen F (2006) Human heat shock protein 60 stimulates vascular smooth muscle cell proliferation through toll-like receptors 2 and 4. Microbes Infect 8:1859–1865
Deocaris CC, Kaul SC, Wadhwa R (2006) On the brotherhood of the mitochondrial chaperones mortalin and heat shock protein 60. Cell Stress Chaperones 11:116–128
Dvorakova L, Ivankova K, Krofta L, Hromadnikova I (2017) Expression profile of heat shock proteins in placental tissues of patients with preterm prelabor rupture of membranes and spontaneous preterm labor with intact membranes. Am J Reprod Immunol 78:e12698
Easton DP, Kaneko Y, Subjeck JR (2000) The hsp110 and Grp1 70 stress proteins: newly recognized relatives of the Hsp70s. Cell Stress Chaperones 5:276–290
Eggert-Kruse W, Scholz S, Kirschfink M, Strowitzki T (2014) Recurrent miscarriages, innate immunity, and autoimmune reaction to chlamydial 60-kDa heat shock protein—is there an association? Fertil Steril 101:1675–1680
El Zowalaty AE, Li R, Zheng Y, Lydon JP, DeMayo FJ, Ye X (2017) Deletion of RhoA in progesterone receptor-expressing cells leads to luteal insufficiency and infertility in female mice. Endocrinology 158:2168–2178
Ellis RJ (1999) Chaperonins. Curr Biol 9:R352
Elustondo P, Martin LA, Karten B (2017) Mitochondrial cholesterol import. Biochim Biophys Acta 1862:90–101
Espinosa-Garcia MT, Strauss JFIII, Martinez F (2000) A trypsin-sensitive protein is required for utilization of exogenous cholesterol for pregnenolone synthesis by placental mitochondria. Placenta 21:654–660
Flores-Herrera O, Uribe A, Garcia-Perez C, Milan R, Martinez F (2002) 5′-p-Fluorosulfonylbenzoyl adenosine inhibits progesterone synthesis in human placental mitochondria. Biochim Biophys Acta 1585:11–18
Friedland JS, Shattock R, Remick DG, Griffin GE (1993) Mycobacterial 65-kD heat shock protein induces release of proinflammatory cytokines from human monocytic cells. Clin Exp Immunol 91:58–62
Galluzzi L, Kepp O, Kroemer G (2012) Mitochondria: master regulators of danger signalling. Nat Rev Mol Cell Biol 13:780–788
Galmiche A, Fueller J (2007) RAF kinases and mitochondria. Biochim Biophys Acta 1773:1256–1262
Gambill BD, Voos W, Kang PJ, Miao B, Langer T, Craig EA, Pfanner N (1993) A dual role for mitochondrial heat shock protein 70 in membrane translocation of preproteins. J Cell Biol 123:109–117
Gharesi-Fard B, Zolghadri J, Kamali-Sarvestani E (2010) Proteome differences of placenta between pre-eclampsia and normal pregnancy. Placenta 31:121–125
Ghosh JC, Dohi T, Kang BH, Altieri DC (2008) Hsp60 regulation of tumor cell apoptosis. J Biol Chem 283:5188–5194
Gotoh T, Terada K, Oyadomari S, Mori M (2004) hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ 11:390–402
Grad I, Picard D (2007) The glucocorticoid responses are shaped by molecular chaperones. Mol Cell Endocrinol 275:2–12
Graham A (2015) Mitochondrial regulation of macrophage cholesterol homeostasis. Free Radic Biol Med 89:982–992
Grunau C, Dettmer R, Behlke J, Bernhardt R (1995) Bovine adrenodoxin – a mitochondrial iron-sulphur protein--binds to chaperonin GroEL. Biochem Biophys Res Commun 210:1001–1008
Gupta RS, Ramachandra NB, Bowes T, Singh B (2008) Unusual cellular disposition of the mitochondrial molecular chaperones Hsp60, Hsp70 and Hsp10. Novartis Found Symp 291:59–68
Habich C, Kempe K, Burkart V, Van Der Zee R, Lillicrap M, Gaston H, Kolb H (2004) Identification of the heat shock protein 60 epitope involved in receptor binding on macrophages. FEBS Lett 568:65–69
Habich C, Kempe K, van der Zee R, Rümenapf R, Akiyama H, Kolb H, Burkart V (2005) Heat shock protein 60: specific binding of lipopolysaccharide. J Immunol 174:1298–1305
Hageman J, Kampinga HH (2009) Computational analysis of the human HSPH/HSPA/DNAJ family and cloning of a human HSPH/HSPA/DNAJ expression library. Cell Stress Chaperones 14:1–21
Hansen JJ, Bross P, Westergaard M, Nielsen MN, Eiberg H, Borglum AD, Mogensen J, Kristiansen K, Bolund L, Gregersen N (2003) Genomic structure of the human mitochondrial chaperonin genes: HSP60 and HSP10 are localised head to head on chromosome 2 separated by a bidirectional promoter. Hum Genet 112:71–77
Harris SF, Shiau AK, Agard DA (2004) The crystal structure of the carboxy-terminal dimerization domain of htpG, the Escherichia coli Hsp90, reveals a potential substrate binding site. Structure 12:1087–1097
Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324–332
He F, Kumar A, Song ZH (2012) Heat shock protein 90 is an essential molecular chaperone for CB2 cannabinoid receptor-mediated signaling in trabecular meshwork cells. Mol Vis 18:2839–2846
Henderson B, Martin AC (2014) Protein moonlighting: a new factor in biology and medicine. Biochem Soc Trans 42:1671–1678
Henderson B, Fares MA, Lund PA (2013) Chaperonin 60: a paradoxical, evolutionarily conserved protein family with multiple moonlighting functions. Biol Rev Camb Philos Soc 88:955–987
Hickey TB, Ziltener HJ, Speert DP, Stokes RW (2010) Mycobacterium tuberculosis employs Cpn60.2 as an adhesin that binds CD43 on the macrophage surface. Cell Microbiol 12:1634–1647
Hightower LE (1980) Cultured animal cells exposed to amino acid analogues or puromycin rapidly synthesize several polypeptides. J Cell Physiol 102:407–427
Hirtreiter AM, Calloni G, Forner F, Scheibe B, Puype M, Vandekerckhove J, Mann M, Hartl FU, Hayer-Hartl M (2009) Differential substrate specificity of group I and group II chaperonins in the aechaeon Methanosarcina mazei. Mol Microbiol 74:1152–1168
Hromadnikova I, Dvorakova L, Kotlabova K, Kestlerova A, Hympanova L, Novotna V, Doucha J, Krofta L (2015) Assessment of placental and maternal stress responses in patients with pregnancy related complications via monitoring of heat shock protein mRNA levels. Mol Biol Rep 42:625–637
Hulce JJ, Cognetta AB, Niphakis MJ, Tully SE, Cravatt BF (2013) Proteome-wide mapping of cholesterol-interacting proteins in mammalian cells. Nat Methods 10:259–264
Issop L, Rone MB, Papadopoulos V (2013) Organelle plasticity and interactions in cholesterol transport and steroid biosynthesis. Mol Cell Endocrinol 371:34–46
Jaattela M (1995) Over-expression of hsp70 confers tumorigenicity to mouse fibrosarcoma cells. Int J Cancer 60:689–693
Jeffery CJ (1999) Moonlighting proteins. Trends Biochem Sci 24:8–11
Jeffery CJ (2017) Protein moonlighting: what is it, and why is it important? Phil Trans R Soc B 373:20160523
Jin H, Ma KD, Hu R, Chen Y, Yang F, Yao J, Li XT, Yang PY (2008) Analysis of expression and comparative profile of normal placental tissue proteins and those in preeclampsia patients using proteomic approaches. Anal Chim Acta 629:158–164
Joab I, Radanyi C, Renoir M, Buchou T, Catelli MG, Binart N, Mester J, Baulieu EE (1984) Common non-hormone binding component in non-transformed chick oviduct receptors of four steroid hormones. Nature 308:850–853
Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE (2009) Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14:105–111
Kaneko Y, Nishiyama H, Nonoguchi K, Higashitsuji H, Kishishita M, Fujita J (1997a) A novel hsp110-related gene, APG-1, that is abundantly expressed in the testis responds to a low temperature heat shock rather than the traditional elevated temperatures. J Biol Chem 272:2640–2645
Kaneko Y, Kimura T, Kishishita M, Noda Y, Fujita J (1997b) Cloning of apg-2 encoding a novel member of heat shock protein 110 family. Gene 189:19–24
Kase S, Parikh JG, Rao NA (2009) Expression of heat shock protein 27 and alpha-crystallins in human retinoblastoma after chemoreduction. Br J Ophthalmol 93:541–544
Kelley WL (1998) The J-domain family and the recruitment of chaperone power. Trends Biochem Sci 23:222–227
Keyse SM, Tyrrell RM (1989) Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci U S A 86:99–103
Khanna A, Aten RF, Behrman HR (1994) Heat shock protein induction blocks hormone-sensitive steroidogenesis in rat luteal cells. Steroids 59:4–9
Khanna A, Aten RF, Behrman HR (1995a) Heat shock protein-70 induction mediates luteal regression in the rat. Mol Endocrinol 9:1431–1440
Khanna A, Aten RF, Behrman HR (1995b) Physiological and pharmacological inhibitors of luteinizing hormone-dependent steroidogenesis induce heat shock protein-70 in rat luteal cells. Endocrinology 136:1775–1781
Kim YN, Kim HK, Warda M, Kim N, Park WS, Prince AB, Jeong DH, Lee DS, Kim KT, Han J (2007) Toward a better understanding of preeclampsia: comparative proteomic analysis of preeclamptic placentas. Proteomics Clin Appl 1:1625–1636
Kim JH, Kim KJ, Rhee YY, Oh S, Cho NY, Lee HS, Kang GH (2013) Expression status of wild-type HSP110 correlates with HSP110 T deletion size and patient prognosis in microsatellite-unstable colorectal cancer. Mod Pathol 27:443–453
Kleinridders A, Lauritzen HPMM, Ussar S, Christensen JH, Mori MA, Bross P, Kahn CR (2013) Leptin regulation of Hsp60 impacts hypothalamic insulin signaling. J Clin Invest 123:4667–4680
Kligman L, Grifo JA, Witkin SS (1996) Expression of the 60 kDa heat shock protein in peritoneal fluids from women with endometriosis: implications for endometriosis-associated infertility. Hum Reprod 11:2736–2738
Lachance C, Bailey JL, Leclerc P (2007) Expression of Hsp60 and Grp78 in the human endometrium and oviduct, and their effect on sperm functions. Hum Reprod 22:2606–2614
Landstein D, Ulmansky R, Naparstek Y (2015) HSP60: a double edge swoed in autimmunity. Oncotarget 6:32299–32300
Lettini G, Maddalena F, Sisinni L, Condelli V, Matassa DS, Costi MP, Simoni D, Esposito F, Landriscina M (2017) TRAP1: a viable therapeutic target for future cancer treatments? Expert Opin Ther Targets 21:805–815
Leung WH, Vong QP, Lin W, Bouck D, Wendt S, Sullivan E, Li Y, Bari R, Chen T, Leung W (2015) PRL-3 mediates the protein maturation of ULBP2 by regulating the tyrosine phosphorylation of HSP60. J Immunol 194:2930–2941
Levinson W, Oppermann H, Jackson J (1980) Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells. Biochim Biophys Acta 606:170–180
Li GC, Shrieve DC (1982) Thermal tolerance and specific protein synthesis in Chinese hamster fibroblasts exposed to prolonged hypoxia. Exp Cell Res 142:464–468
Li C, Liu D, Yuan Y, Huang S, Shi M, Tao K, Feng W (2010) Overexpresion of APG-2 increases cell proliferation and protects from oxidative damage in BaF3-BCR/ABL cells. Int J Oncol 36:899–904
Li L, Wu J, Luo M, Sun Y, Wang G (2016) The effect of heat stress on gene expression, synthesis of steroids, and apoptosis in bovine granulosa cells. Cell Stress Chaperones 21:467–475
Lin CY, Hu CT, Cheng CC, Lee MC, Pan SM, Lin TY, Wu WS (2016) Oxidation of heat shock protein 60 and protein disulfide isomerase activates ERK and migration of human hepatocellular carcinoma HepG2. Oncotarget 7:11067–11082
Liu Z, Stocco DM (1997) Heat shock-induced inhibition of acute steroidogenesis in MA-10 cells is associated with inhibition of the synthesis of the steroidogenic acute regulatory protein. Endocrinology 138:2722–2728
Lund PA (2001) Microbial molecular chaperones. Adv Microb Physiol 44:93–140
Luo W, Sun W, Taldone T, Rodina A, Chiosis G (2010) Heat shock protein 90 in neurodegenerative diseases. Mol Neurodegener 5:24
Mahlke K, Pfanner N, Martin J, Horwich AL, Hartl FU, Neupert W (1990) Sorting pathways of mitochondrial inner membrane proteins. Eur J Biochem 192:551–555
Mandal K, Foteinos G, Jahangiri M, Xu Q (2005) Role of antiheat shock protein 60 autoantibodies in atherosclerosis. Lupus 14:742–746
Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schütz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM (1995) The nuclear receptor superfamily: the second decade. Cell 83:835–839
Mani M, Chen C, Amblee V, Liu H, Mathur T, Zwicke G, Zabad S, Patel B, Thakkar J, Jeffery CJ (2015) MoonProt: a database for proteins that are known to moonlight. Nucleic Acids Res 43:D277–D282
Marom M, Dayan D, Demishtein-Zohary K, Mokranjac D, Neupert W, Azem A (2011) Direct interaction of mitochondrial targeting presequences with purified components of the TIM23 protein complex. J Biol Chem 286:43809–43815
Martinez F, Olvera-Sanchez S, Esparza-Perusquia M, Gomez-Chang E, Flores-Herrera O (2015) Multiple functions of syncytiotrophoblast mitocondria. Steroids 103:11–22
Matsuda M, Sasaki A, Shimizu K, Kamada Y, Noguchi S, Hiramatsu Y, Nakatsuka M (2017) Increased anti-HSP60 and anti-HSP70 antibodies in women with unexplained recurrent pregnancy loss. Acta Med Okayama 71:201–208
Meghji S, Lillicrap M, Maguire M, Tabona P, Gaston JS, Poole S, Henderson B (2003) Human chaperonin 60 (Hsp60) stimulates bone resorption: structure/function relationships. Bone 33:419–425
Meng Q, Li BX, Xiao X (2018) Toward developing chemical modulators of Hsp60 as potential therapeutics. Front Mol Biosci 5:35
Merbl Y, Zucker-Toledano M, Quintana FJ, Cohen IR (2007) Newborn humans manifest autoantibodies to defined self molecules detected by antigen microarray informatics. J Clin Invest 117:712–718
Milioti N, Bermudez-Fajardo A, Penichet ML, Oviedo-Orta E (2008) Antigen-induced immunomodulation in the pathogenesis of atherosclerosis. Clin Dev Immunol 2008:723539
Miller WL (2013) Steroid hormone synthesis in mitochondria. Mol Cell Endocrinol 379:62–73
Miller WL, Bose HS (2011) Early steps in steroidogenesis: intracellular cholesterol trafficking. J Lipid Res 52:2111–2135
Mine K, Katayama A, Matsumura T, Nishino T, Kuwabara Y, Ishikawa G, Murata T, Sawa R, Otsubo Y, Shin S, Takeshita T (2007) Proteome analysis of human placentae: pre-eclampsia versus normal pregnancy. Placenta 28:676–687
Mitra A, Shevde LA, Samant RS (2009) Multi-faceted role of HSP40 in cancer. Clin Exp Metastasis 26:559–567
Miyata S, Mizuno T, Koyama Y, Katayama T, Tohyama M (2013) The endoplasmic reticulum-resident chaperone heat shock protein 47 protects the Golgi apparatus from the effects of O-glycosylation inhibition. PLoS One 8:e69732
Mohamed BA, Barakat AZ, Zimmermann WH, Bittner RE, Muhlfeld C, Hunlich M, Engel W, Maier LS, Adham IM (2012) Targeted disruption of Hspa4 gene leads to cardiac hypertrophy and fibrosis. J Mol Cell Cardiol 53:459–468
Molvarec A, Derzsy Z, Kocsis J, Bőze T, Nagy B, Balogh K, Makó V, Cervenak L, Mézes M, Karádi I, Prohászka Z, Rigó JJ (2009) Circulating anti-heat-shock-protein antibodies in normal pregnancy and preeclampsia. Cell Stress Chaperones 14:491–498
Molvarec A, Tamasi L, Losonczy G, Madach K, Prohaszka Z, Rigo JJ (2010) Circulating heat shock protein 70 (HSPA1A) in normal and pathological pregnancies. Cell Stress Chaperones 15:237–247
Monaghan RM, Whitmarsh AJ (2015) Mitochondrial proteins moonlighting in the nucleus. Trends Biochem Sci 40:728–735
Monreal-Flores J, Espinosa-Garcia MT, Garcia-Regalado A, Arechavaleta-Velasco F, Martinez F (2017) The heat shock protein 60 promotes progesterone synthesis in mitochondria of JEG-3 cells. Reprod Biol 17:154–161
Mookerjee-Basu J, Vantourout P, Martinez LO, Perret B, Collet X, Périgaud C, Peyrottes S, Champagne E (2010) F1-adenosine triphosphatase displays properties characteristic of an antigen presentation molecule for Vgamma9Vdelta2 T cells. J Immunol 184:6920–6928
Murphy ME (2013) The HSP70 family and cancer. Carcinogenesis 34:1181–1188
Murphy BD, Lalli E, Walsh LP, Liu Z, Soh J, Stocco DM, Sassone-Corsi P (2001) Heat shock interferes with steroidogenesis by reducing transcription of the steroidogenic acute regulatory protein gene. Mol Endocrinol 15:1255–1263
Naaby-Hansen S, Herr JC (2010) Heat shock proteins on the human sperm surface. J Reprod Immunol 84:32–40
Nadin SB, Vargas-Roig LM, Cuello-Carrion FD, Ciocca DR (2003) Deoxyribonucleic acid damage induced by doxorubicin in peripheral blood mononuclear cells: possible roles for the stress response and the deoxyribonucleic acid repair process. Cell Stress Chaperones 8:361–372
Nagumo Y, Kakeya H, Shoji M, Hayashi Y, Dohmae N, Osada H (2005) Epolactaene binds human Hsp60 Cys442 resulting in the inhibition of chaperone activity. Biochem J 387:835–840
Nanbu K, Konishi I, Mandai M, Kuroda H, Hamid AA, Komatsu T, Mori T (1998) Prognostic significance of heat shock proteins HSP70 and HSP90 in endometrial carcinomas. Cancer Detect Prev 22:549–555
Navarrete J, Flores-Herrera O, Uribe A, Martínez F (1999) Differences in cholesterol incorporation into mitochondria from hepatoma AS-30D and human term placenta. Placenta 20:285–291
Neuer A, Spandorfer S, Giraldo P, Mele C, Liu HC, Marzusch K, Kneissl D, Witkin SS (1997) Immune sensitization to the 60 kD heat shock protein and pregnancy outcome. Infect Dis Obstet Gynecol 5:154–157
Neuer A, Spandorfer SD, Giraldo P, Dieterle S, Rosenwaks Z, Witkin SS (1999) The role of heat shock proteins in reproduction. Hum Reprod Update 6:149–159
Ohashi R, Mu H, Yao Q, Chen C (2004) Atherosclerosis: immunopathogenesis and immunotherapy. Med Sci Monit 10:RA255–RA260
Oka S, Shiraishi K, Fujimoto M, Katiyar A, Takii R, Nakai A, Matsuyama H (2017) Role of heat shock factor 1 in conserving cholesterol transportation in leydig cell steroidogenesis via steroidogenic acute regulatory protein. Endocrinology 158:2648–2658
Olvera-Sanchez S, Espinosa-Garcia MT, Monreal J, Flores-Herrera O, Martinez F (2011) Mitochondrial heat shock protein participates in placental steroidogenesis. Placenta 32:222–229
Omori H, Otsu M, Suzuki A, Nakayama T, Akama K, Watanabe M, Inoue N (2013) Effects of heat shock on survival, proliferation and differentiation of mouse neural stem cells. Neurosci Res 79:13–21
Papadopoulos V, Miller WL (2012) Role of mitochondria in steroidogenesis. Best Pract Res Clin Endocrinol Metab 26:771–790
Pockley AG, Bulmer J, Hanks BM, Wright BH (1999) Identification of human heat shock protein 60 (Hsp60) and anti-Hsp60 antibodies in the peripheral circulation of normal individuals. Cell Stress Chaperones 4:29–35
Prasad TK, Hack E, Hallberg RL (1990) Function of the maize mitochondrial chaperonin hsp60: specific association between hsp60 and newly synthesized F1 ATPase alpha subunits. Mol Cell Biol 10:3979–3986
Prasad M, Pawlak KJ, Burak WE, Perry EE, Marshall B, Whittal RM, Bose HS (2017) Mitochondrial metabolic regulation by GRP78. Sci Adv 3:e1602038
Pratt WB, Morishima Y, Murphy M, Harrell M (2006) Chaperoning of glucocorticoid receptors. Handb Exp Pharmacol 172:111–138
Quintana FJ, Cohen IR (2011) The HSP60 immune system network. Trends Immunol 32:89–95
Ranford J, Henderson B (2002) Chaperonins in disease: mechanisms, models and therapies. J Clin Pathol Mol Pathol 55:209–213
Rani N, Bharti S, Manchanda M, Nag TC, Ray R, Chauhan SS, Kumari S, Arya DS (2013) Regulation of heat shock proteins 27 and 70, p-Akt/p-eNOS and MAPKs by Naringin dampens myocardial injury and dysfunction in vivo after ischemia/reperfusion. PLoS One 8:e82577
Rappa F, Unti E, Baiamonte P, Cappello F, Scibetta N (2013) Different immunohistochemical levels of Hsp60 and Hsp70 in a subset of brain tumors and putative role of Hsp60 in neuroepithelial tumorigenesis. Eur J Histochem 57:e20
Ravagnan L, Gurbuxani S, Susin SA, Maisse C, Daugas E, Zamzami N, Mak T, Jaattela M, Penninger JM, Garrido C, Kroemer G (2001) Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol 3:839–843
Ritossa F (1996) Discovery of the heat shock response. Cell Stress Chaperones 1:97–98
Rohl A, Rohrberg J, Buchner J (2013) The chaperone Hsp90: changing partners for demanding clients. Trends Biochem Sci 38:253–262
Rone MB, Liu J, Blonder J, Ye X, Veenstra TD, Young JC, Papadopoulos V (2009) Targeting and insertion of the cholesterol-binding translocator protein into the outer mitochondrial membrane. Biochemistry 48:6909–6920
Roostaee A, Barbar E, Lavigne P, LeHoux JG (2009) The mechanism of specific binding of free cholesterol by the steroidogenic acute regulatory protein: evidence for a role of the C-terminal α-helix in the gating of the binding site. Biosci Rep 29:89–101
Saleh A, Srinivasula SM, Balkir L, Robbins PD, Alnemri ES (2000) Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat Cell Biol 2:476–483
Sanderson JT (2006) The steroid hormone biosynthesis pathway as a target for endocrine-disrupting chemicals. Toxicol Sci 94:3–21
Seigneuric R, Mjahed H, Gobbo J, Joly AL, Berthenet K, Shirley S, Garrido C (2011) Heat shock proteins as danger signals for cancer detection. Front Oncol 1:37
Shah M, Stanek J, Handwerger S (1998) Differential localization of heat shock proteins 90, 70, 60 and 27 in human decidua and placenta during pregnancy. Histochem J 30:509–518
Shamaei-Tousi A, Steptoe A, O'Donnell K, Palmen J, Stephens JW, Hurel SJ, Marmot M, Homer K, D'Aiuto F, Coates AR, Humphries SE, Henderson B (2007) Plasma heat shock protein 60 and cardiovascular disease risk: the role of psychosocial, genetic, and biological factors. Cell Stress Chaperones 12:384–392
Shi Y, Thomas JO (1992) The transport of proteins into the nucleus requires the 70-kilodalton heat shock protein or its cytosolic cognate. Mol Cell Biol 12:2186–2192
Shi Z, Long W, Zhao C, Guo X, Shen R, Ding H (2013) Comparative proteomics analysis suggests that placental mitochondria are involved in the development of pre-eclampsia. PLoS One 8:e64351
Shin JK, Baek JC, Kang MY, Park JK, Lee SA, Lee JH, Choi WS, Paik WY (2011) Proteomic analysis reveals an elevated expression of heat shock protein 27 in preeclamptic placentas. Gynecol Obstet Investig 71:151–157
Skjærven L, Cuellar J, Martinez A, Valpuesta JM (2015) Dynamics, flexibility, and allostery in molecular chaperonins. FEBS Lett 589:2522–2532
Slaby O, Sobkova K, Svoboda M, Garajova I, Fabian P, Hrstka R, Nenutil R, Sachlova M, Kocakova I, Michalek J, Smerdova T, Knoflickova D, Vyzula R (2009) Significant overexpression of Hsp110 gene during colorectal cancer progression. Oncol Rep 21:1235–1241
Soltys BJ, Gupta RS (1996) Immunoelectron microscopic localization of the 60-kDa heat shock chaperonin protein (Hsp60) in mammalian cells. Exp Cell Res 222:16–27
Soltys BJ, Gupta RS (1997) Cell surface localization of the 60 kDa heat shock chaperonin protein (hsp60) in mammalian cells. Cell Biol Int 21:315–320
Somji S, Todd JH, Sens MA, Garrett SH, Sens DA (2000) Expression of heat shock protein 60 in human proximal tubule cells exposed to heat, sodium arsenite and CdCl(2). Toxicol Lett 115:127–136
Sterrenberg JN, Blatch GL, Edkins AL (2011) Human DNAJ in cancer and stem cells. Cancer Lett 312:129–142
Sullivan CS, Pipas JM (2002) T antigens of simian virus 40: molecular chaperones for viral replication and tumorigenesis. Microbiol Mol Biol Rev 66:179–202
Sun X, Fontaine JM, Bartl I, Behnam B, Welsh MJ, Benndorf R (2007a) Induction of Hsp22 (HspB8) by estrogen and the metalloestrogen cadmium in estrogen receptor-positive breast cancer cells. Cell Stress Chaperones 12:307–319
Sun LZ, Yang NN, De W, Xiao YS (2007b) Proteomic analysis of proteins differentially expressed in preeclamptic trophoblasts. Gynecol Obstet Investig 64:17–23
Tabibzadeh S, Broome J (1999) Heat shock proteins in human endometrium throughout the menstrual cycle. Infect Dis Obstet Gynecol 7:5–9
Tabibzadeh S, Kong QF, Satyaswaroop PG, Babaknia A (1996) Heat shock proteins in human endometrium throughout the menstrual cycle. Hum Reprod 11:633–640
Taylor M, Navarro-Garcia F, Huerta J, Burress H, Maseey S, Ireton K, Teter K (2010) Hsp90 is required for transfer of the cholera toxin A1 subunit from the endoplasmic reticulum to the cytosol. J Biol Chem 285:31261–31267
Trapasso F, Pichiorri F, Gaspari M, Palumbo T, Aqeilan RI, Gaudi E, Okumura H, Luliano R, Di Leva G, Fabbri M, Birk DE, Raso C, Green-Church K, Spagnoli LG, Venuta S, Huebner K, Croce CM (2008) Fhit interaction with ferredoxin reductase triggers generation of reactive oxygen species and apoptosis of cancer cells. J Biol Chem 283:13736–13744
Tsai YP, Teng SC, Wu KJ (2008) Direct regulation of HSP60 expression by c-MYC induces transformation. FEBS Lett 582:4083–4088
Tsai YP, Yang MH, Huang CH, Chang SY, Chen PM, Liu CJ, Teng SC, Wu KJ (2009) Interaction between HSP60 and beta-catenin promotes metastasis. Carcinogenesis 30:1049–1057
Tuccinardi D, Fioriti E, Manfrini S, D'Amico E, Pozzilli P (2011) DiaPep277 peptide therapy in the context of other immune intervention trials in type 1 diabetes. Expert Opin Biol Ther 11:1233–1240
Uribe A, Strauss JF III, Martínez F (2003) Contact sites from human placental mitochondria: characterization and role in progesterone synthesis. Placenta 413:172–181
Vos MJ, Hageman J, Carra S, Kampinga HH (2008) Structural and functional diversities between members of the human HSPB, HSPH, HSPA, and DNAJ chaperone families. Biochemistry 47:7001–7011
Wang W, Jeffery CJ (2016) An analysis of surface proteomics results reveals novel candidates for intracellular/surface moonlighting proteins in bacteria. Mol BioSyst 12:1420–1431
Wang F, Shi Z, Wang P, You W, Liang G (2013) Comparative proteome profile of human placenta from normal and preeclamptic pregnancies. PLoS One 8:e78025
Whitesell L, Lindquist SL (2005) HSP90 and the chaperoning of cancer. Nat Rev Cancer 5:761–772
Witkin SS (1999) Immunity to heat shock proteins and pregnancy outcome. Infect Dis Obstet Gynecol 7:35–38
Woo SH, An S, Lee HC, Jin HO, Seo SK, Yoo DH, Lee KH, Rhee CH, Choi EJ, Hong SI, Park IC (2009) A truncated form of p23 down-regulates telomerase activity via disruption of Hsp90 function. J Biol Chem 284:30871–30880
Wyttenbach A, Carmichael J, Swartz J, Furlong RA, Narain Y, Rankin J, Rubinsztein DC (2000) Effects of heat shock, heat shock protein 40 (HDJ-2), and proteasome inhibition on protein aggregation in cellular models of Huntington's disease. Proc Natl Acad Sci U S A 97:2898–2903
Xiao Q, Mandal K, Schett G, Mayr M, Wick G, Oberhollenzer F, Willeit J, Kiechl S, Xu Q (2005) Association of serum-soluble heat shock protein 60 with carotid atherosclerosis: clinical significance determined in a follow-up study. Stroke 36:2571–2576
Xu Y, Lindquist S (1993) Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc Natl Acad Sci U S A 90:7074–7078
Yagita Y, Kitagawa K, Taguchi A, Ohtsuki T, Kuwabara K, Mabuchi T, Matsumoto M, Yanagihara T, Hori M (1999) Molecular cloning of a novel member of the HSP110 family of genes, ischemia-responsive protein 94 kDa (irp94), expressed in rat brain after transient forebrain ischemia. J Neurochem 72:1544–1551
Yan FQ, Wang JQ, Tsai YP, Wu KJ (2015) HSP60 overexpression increases the protein levels of the p110a subunit of phosphoinositide 3-kinase and c-Myc. Clin Exp Pharmacol Physiol 42:1092–1097
Yang JI, Kong TW, Kim HS, Kim HY (2015) The proteomic analysis of human placenta with pre-eclampsia and normal pregnancy. J Korean Med Sci 30:770–778
Zhang X, Pang H, Wu Z, Jian J (2011) Molecular characterization of heat shock protein 70 gene transcripts during Vibrio harveyi infection of humphead snapper, Lutjanus sanguineus. Fish Physiol Biochem 37:897–910
Ziegert M, Witkin SS, Sziller I, Alexander H, Brylla E, Hirtig W (1999) Heat shock proteins and heat shock protein-antibody complexes in placental tissues. Infect Dis Obstet Gynecol 7:180–185
Acknowledgements
This work was partially supported by Grants IN211912, IN211715 and IN215518 (FM), IN222617 (OFH) from Dirección General de Apoyo al Personal Académico (UNAM), and 168025 (FM) from Consejo Nacional de Ciencia y Tecnología, México.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Olvera-Sanchez, S., Monreal-Flores, J., Flores-Herrera, O., Martinez, F. (2019). Role of HSP60 in Steroidogenesis and Reproduction. In: Asea, A., Kaur, P. (eds) Heat Shock Protein 60 in Human Diseases and Disorders. Heat Shock Proteins, vol 18. Springer, Cham. https://doi.org/10.1007/978-3-030-23154-5_20
Download citation
DOI: https://doi.org/10.1007/978-3-030-23154-5_20
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-23153-8
Online ISBN: 978-3-030-23154-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)