Advertisement

Heat Shock Protein 60 (HSP60): Role in Skeletal Muscle Diseases and Novel Prospects for Therapy

  • Richa RathorEmail author
  • Geetha Suryakumar
  • Som Nath Singh
  • Bhuvnesh Kumar
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 18)

Abstract

Eukaryotic Hsp60 is also known as mitochondrial chaperones (Chaperonin, Cpn60) as earlier it was considered to be present in mitochondria only. Last few years it has become clear that it is also present in cytosol, cell surface, extracellular space and in the peripheral blood. Hsp60 plays a vital role in quality control of proteins. It interacts with Hsp10 (resides in mitochondria, also named as Cpn10) to prepare native conformational protein from nascent polypeptides in the presence of ATP. Some other newly identified functions of Hsp60 include cell survival and proliferation. Hsp60 has significant role in various skeletal muscle wasting diseases like sarcopenia, cancer cachexia, sepsis, denervation, burns, and chronic obstructive pulmonary disease. The present chapter describes a brief representative research efforts aimed to establish the role of Hsp60 in various skeletal muscle wasting conditions with the purpose to illustrate possible protective and therapeutic implications for developing novel approach to rectify them.

Keywords

Cytoprotection High altitude Hsp60 Proteostasis Quality control Skeletal muscle 

Abbreviations

HSBP1

Heat shock protein binding factor 1

HSEs

Heat shock elements

HSF1

Heat shock factor transcription factor

HSP

Heat shock family

Hsp

Heat shock proteins

Hsp60

Heat shock protein60

IGF1

Insulin growth factor-1

LMF

Lipid mobilising factor

MAPK

Mitogen-activated protein kinase

mTOR

Mammalian target of rapamycin

TLRs

Toll like receptors

UPS

Unfolded protein response

Notes

Acknowledgements

The authors are thankful to Dr. Bhuvnesh Kumar, Director, DIPAS, for his constant support and encouragement. The study was supported by the Defence Research and Development Organisation, Ministry of Defence, Government of India.

References

  1. Agrawal A, Rathor R, Suryakumar G (2017) Oxidative protein modification alters proteostasis under acute hypobaric hypoxia in skeletal muscles: a comprehensive in vivo study. Cell Stress Chaperones 22(3):429–443PubMedPubMedCentralCrossRefGoogle Scholar
  2. Agrawal A, Rathor R, Kumar R, Suryakumar G, Ganju L (2018) Role of altered proteostasis network in chronic hypobaric hypoxia induced skeletal muscle atrophy. PLoS One 13(9):e0204283PubMedPubMedCentralCrossRefGoogle Scholar
  3. Andersen KJ (2004) Oxidative stress in neurodegeneration: cause or consequence? Nat Rev Neurosci 5:S18–S25CrossRefGoogle Scholar
  4. Argilés JM, Busquets S, García-Martínez C, López-Soriano FJ (2005) Mediators involved in the cancer anorexia-cachexia syndrome: past, present, and future. Nutrition 21:977–985PubMedCrossRefGoogle Scholar
  5. Atre N, Thomas L, Mistry R, Pathak K, Chiplunkar S (2006) Role of nitric oxide in heat shock protein induced apoptosis of gamma delta T cells. Int J Cancer 119:1368–1376PubMedCrossRefGoogle Scholar
  6. Auluck PK, Chan HY, Trojanowski JQ, Lee VM, Bonini NM (2002) Chaperone suppression of alpha-synuclein toxicity in a Drosophila model for Parkinson's disease. Science 295:865–868PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bach JR, O’Brien J, Krotenberg R, Alba AS (1987) Management of end stage respiratory failure in Duchenne muscular dystrophy. Muscle Nerve 10:177–182PubMedCrossRefGoogle Scholar
  8. Barbieri E, Sestili P (2012) Reactive oxygen species in skeletal muscle signaling. J Sig Transduct 2012:982794Google Scholar
  9. Barbieri E, Sestili P, Vallorani L, Guescini M, Calcabrini C, Gioacchini AM, Annibalini G, Lucertini F, Piccoli G, Stocchi V (2014) Mitohormesis in muscle cells: a morphological, molecular, and proteomic approach. Muscle Ligaments Tendons J 3(4):254–266CrossRefGoogle Scholar
  10. Barone R, Macalusa F, Sangiogi C, D’Amico D, Gammazza AM, Campanella C, Cappello F, Zummo G, Farina F (2016) Hsp60 and interleukins expression in the skeletal muscle and its implications in exercise and cachexia. Ital J Anat Embryol 121(1):26Google Scholar
  11. Beccafico S, Puglielli C, Pietrangelo T, Bellomo R, Fanò G, Fulle S (2007) Age-dependent effects on functional aspects in human satellite cells. Ann N Y Acad Sci 1100:345–352PubMedCrossRefGoogle Scholar
  12. Bosaeus I, Daneryd P, Svanberg E, Lundholm K (2001) Dietary intake and resting energy expenditure in relation to weight loss in unselected cancer patients. Int J Cancer 93:380–383PubMedCrossRefGoogle Scholar
  13. Bosutti A, Toigo G, Ciocchi B, Situlin R, Guarnieri G, Biolo G (2002) Regulation of muscle cathepsin B proteolytic activity in protein-depleted patients with chronic diseases. Clin Nutr 21(5):373–378PubMedCrossRefGoogle Scholar
  14. Brodsky JL, Chiosis G (2006) Hsp70 molecular chaperones: emerging roles in human disease and identification of small molecule modulators. Curr Top Med Chem 6:1215–1225PubMedCrossRefGoogle Scholar
  15. Busquets S, García-Martínez C, Alvarez B, Carbó N, López-Soriano FJ, Argilés JM (2000) Calpain-3 gene expression is decreased during experimental cancer cachexia. Biochim Biophys Acta 1475(1):5–9PubMedCrossRefGoogle Scholar
  16. 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 func- tions involve differential interactions with caspase-3. J Biol Chem 282:31289–31301PubMedCrossRefGoogle Scholar
  17. Chaudhury P, Suryakumar G, Prasad R, Singh SM, Ali S, Ilavazhagan G (2012) Chronic hypobaric hypoxia mediated skeletal muscle atrophy: role of ubiquitin–proteasome pathway and calpains. Mol Cell Biochem 364:101–113CrossRefGoogle Scholar
  18. Chen W, Syldath U, Bellmann K, Burkart V, Kolb H (1999) Human 60-kDa heat-shock protein: a danger signal to the innate immune system. J Immunol 162:3212–3219PubMedPubMedCentralGoogle Scholar
  19. Chen W, Wang J, Shao C, Liu S, Yu Y, Wang Q, Cao X (2006) Efficient induction of antitumor T cell immunity by exosomes derived from heat-shocked lymphoma cells. Eur J Immunol 36:1598–1607PubMedCrossRefGoogle Scholar
  20. Chung L, Ng YC (2006) Age-related alternations in expression of apoptosis regulatory proteins and heat shock proteins in rat skeletal muscle. BBA-Mol Basis Dis 1762(1):103–109CrossRefGoogle Scholar
  21. Colotti C, Cavallini G, Vitale RL, Donati A, Maltinti M, Del Ry S, Bergamini E, Giannessi D (2005) Effects of aging and anti-aging caloric restrictions on carbonyl and heat shock protein levels and expression. Biogerontology 6:397–406PubMedCrossRefGoogle Scholar
  22. Csermely P (1999) The “chaperone-percolator” model: a possible molecular mechanism of Anfinsen-cage type chaperone action. BioEssays 21:959–965PubMedCrossRefGoogle Scholar
  23. Czarnecka AM, Campanella C, Zummo G, Cappello F (2006) Heat shock protein 10 and signal transduction: a “capsula eburnea” of carcinogenesis? Cell Stress Chaperones 11:287–294PubMedPubMedCentralCrossRefGoogle Scholar
  24. Dargelos E, Brulé C, Combaret L, Hadj-Sassi A, Dulong S, Poussard S, Cottin P (2007) Involvement of the calcium-dependent proteolytic system in skeletal muscle aging. Exp Gerontol 42(11):1088–1098PubMedCrossRefGoogle Scholar
  25. Davies KE, Nowak KJ (2006) Molecular mechanisms of muscular dystrophies: old and new players. Nat Rev Mol Cell Biol 7:762–773PubMedCrossRefGoogle Scholar
  26. DeJong CH, Busquets S, Moses AG, Schrauwen P, Ross JA, Argiles JM, Fearon KC (2005) Systemic inflammation correlates with increased expression of skeletal muscle ubiquitin but not uncoupling proteins in cancer cachexia. Oncol Rep 14(1):257–263PubMedGoogle Scholar
  27. Deocaris CC, Kaul SC, Wadhwa R (2006) On the brotherhood of the mitochondrial chaperones mortalin and heat shock protein 60. Cell Stress Chaperones 11:116–128PubMedPubMedCentralCrossRefGoogle Scholar
  28. DeSantis ME, Leung EH, Sweeny EA, Jackrel ME, Cushman-Nick M, Neuhaus-Follini A, Vashist S, Sochor MA, Knight MN, Shorter J (2012) Operational plasticity enables hsp104 to disaggregate diverse amyloid and nonamyloid clients. Cell 151:778–793PubMedPubMedCentralCrossRefGoogle Scholar
  29. Emery AE (1990) Dystrophin function. Lancet 335:1289PubMedCrossRefGoogle Scholar
  30. Emery AE (1993) Duchenne muscular dystrophy–Meryon’s disease. Neuromuscul Disord 3:263–266PubMedCrossRefGoogle Scholar
  31. Evans WJ, Morley JE, Argilés J, Bales C, Baracos V, Guttridge D, Jatoi A, Kalantar-Zadeh K, Lochs H, Mantovani G, Marks D, Mitch WE, Muscaritoli M, Najand A, Ponikowski P, Rossi Fanelli F, Schambelan M, Schols A, Schuster M, Thomas D, Wolfe R, Anker SD (2008) Cachexia: a new definition. Clin Nutr 27(6):793–799PubMedCrossRefGoogle Scholar
  32. Fearon KC, Voss AC, Hustead DS, Cancer Cachexia Study Group (2006) Definition of cancer cachexia: effect of weight loss, reduced food intake, and systemic inflammation on functional status and prognosis. Am J Clin Nutr 83:1345–1350PubMedCrossRefGoogle Scholar
  33. Febbraio MA, Koukoulas I (2000) HSP72 gene expression progressively increases in human skeletal muscle during prolonged, exhaustive exercise. J Appl Physiol 89:1055–1060PubMedCrossRefGoogle Scholar
  34. Feng H, Zeng Y, Graner MW, Katsanis E (2002) Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells. Blood 100:4108–4115PubMedCrossRefGoogle Scholar
  35. Ghosh JC, Dohi T, Kang BH, Altieri DC (2008) Hsp60 regulation of tumor cell apoptosis. J Biol Chem 283:5188–5194.  https://doi.org/10.1074/jbc.M705904200CrossRefGoogle Scholar
  36. Graul AI, Stringer M, Sorbera LC (2016) Drugs Today 52(9):519PubMedCrossRefGoogle Scholar
  37. Guiraud S, Aartsma-Rus A, Vieira NM, Davies KE, van Ommen GJ, Kunkel LM (2015) The pathogenesis and therapy of muscular dystrophies. Ann Rev Genom Hum Genet 16:281–308CrossRefGoogle Scholar
  38. Guiraud S, Edwards B, Squire SE, Babbs A, Shah N, Berg A, Chen H, Davies KE (2017) Identification of serum protein biomarkers for utrophin based DMD therapy. Sci Rep 7:43697PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gupta S, Knowlton AA (2007) Hsp60 trafficking in adult cardiac myocytes: role of exosomal pathway. Am J Physiol Heart Circ Physiol 292:3052–3056CrossRefGoogle Scholar
  40. Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324–332PubMedPubMedCentralCrossRefGoogle Scholar
  42. Haslbeck M, Vierling E (2015) A first line of stress defense: small heat shock proteins and their function in protein homeostasis. J Mol Biol 427:1537–1548PubMedPubMedCentralCrossRefGoogle Scholar
  43. Iannuzzi-Sucich M, Prestwood KM, Kenny AM (2002) Prevalence of sarcopenia and predictors of skeletal muscle mass in healthy, older men and women. J Gerontol A Biol Sci Med Sci 57(12):M772–M777PubMedCrossRefGoogle Scholar
  44. Itoh H, Komatsuda A, Ohtani H, Wakui H, Imai H, Sawada K, Otaka M, Ogura M, Suzuki A, Hamada F (2002) Mammalian HSP60 is quickly sorted into the mitochondria under conditions of dehydration. Eur J Biochem 269:5931–5938PubMedCrossRefGoogle Scholar
  45. Jain K, Suryakumar G, Prasad R, Ganju L (2013) Differential activation of myocardial ER stress response: a possible role in hypoxic tolerance. Int J Cardiol 168(5):667–677CrossRefGoogle Scholar
  46. Jain K, Suryakumar G, Ganju L, Singh SB (2014) Differential hypoxic tolerance is mediated by activation of heat shock response and nitric oxide pathway. Cell Stress Chaperones 19(6):801–812PubMedPubMedCentralCrossRefGoogle Scholar
  47. Joseph AM, Adhihwtty PJ, Buford TW, Wohlgemuth SE, Lees HA, Nguyen LMD, Aranda JM, Sandesara BD, Pahor M, Manini TM, Marzetti E, Leeuwenburgh C (2012) The impact of aging on mitochondrial function and biogenesis pathways in skeletal muscle of sedentary high- and low-functioning elderly individuals. Aging Cell 11(5):801–809PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kastle M, Grune T (2012) Interactions of the proteasomal system with chaperones: protein triage and protein quality control. Prog Mol Biol Transl Sci 109:113–160PubMedCrossRefGoogle Scholar
  49. Khal J, Hine AV, Fearon KCH, Dejong CHC, Tisdale MJ (2005) Increased expression of proteasome subunits in skeletal muscle of cancer patients with weight loss. Int J Biochem Cell Biol 37(10):2196–2206PubMedCrossRefGoogle Scholar
  50. Khassaf M, Child RB, McArdle A, Brodie DA, Esanu C, Griffiths RD, Jackson MJ (2001) Time course of responses of human skeletal muscle to oxidative stress induced by nondamaging exercise. J Appl Physiol 90:1031–1035PubMedCrossRefGoogle Scholar
  51. Kim J, Nueda A, Meng YH, Dynan WS, Mivechi NF (1997) Analysis of the phosphorylation of human heat shock transcription factor-1 by MAP kinase family members. J Cell Biochem 67:43–54PubMedCrossRefGoogle Scholar
  52. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU (2013) Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 82:323–355PubMedCrossRefGoogle Scholar
  53. Kirchengast S, Huber J (2009) Gender and age differences in lean soft tissue mass and sarcopenia among healthy elderly. Anthropol Anz 67(2):139–151PubMedCrossRefGoogle Scholar
  54. Knauf U, Newton EM, Kyriakis J, Kingston RE (1996) Repression of human heat shock factor 1 activity at control temperature by phosphorylation. Genes Dev 10:2782–2793PubMedCrossRefGoogle Scholar
  55. Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186PubMedCrossRefGoogle Scholar
  56. Landi F, Liperoti R, Fusco D, Mastropaolo S, Quattrociocchi D, Proia A, Tosato M, Bernabei R, Onder G (2012) Sarcopenia and mortality among older nursing home residents. J Am Med Dir Assoc 13:121–126PubMedCrossRefGoogle Scholar
  57. Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, Corsi AM, Rantanen T, Guralnik JM, Ferrucci L (2003) Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol 95(5):1851–1860PubMedCrossRefGoogle Scholar
  58. Macario AJL, de Macario CE (2007) Molecular chaperones: multiple functions, pathologies and potential applications. Front Biosci 12:2588–2600PubMedCrossRefGoogle Scholar
  59. MacDonald N, Easson AM, Mazurak VC, Dunn GP, Baracos VE (2003) Understanding and managing cancer cachexia. J Am Coll Surg 197(1):143–161PubMedCrossRefGoogle Scholar
  60. Maglara AA, Vasilaki A, Jackson MJ, McArdle A (2003) Damage to developing mouse skeletal muscle myotubes in culture: protective effect of heat shock proteins. J Physiol 548:837–846PubMedPubMedCentralCrossRefGoogle Scholar
  61. Marber MS (1994) Stress proteins and myocardial protection. Clin Sci (Lond) 86:375–381CrossRefGoogle Scholar
  62. McArdle A, Pattwell D, Vasilaki A, Griffiths RD, Jackson MJ (2001) Contractile activity-induced oxidative stress: cellular origin and adaptive responses. Am J Physiol Cell Physiol 280:C621–C627PubMedCrossRefGoogle Scholar
  63. McMillan DC, Preston T, Fearon KCH, Burns HJG, Slater C, Shenkin A (1994) Protein synthesis in cancer patients with inflammatory response: investigations with [N]glycine. Nutrition 10(3):232–240PubMedGoogle Scholar
  64. McMulen CA, Ferry AL, Gamboa JL, Andrade FH, Dupont-Versteegden EE (2009) Age-related changes of cell death pathways in rat extraocular muscle. Exp Gerontol 44:20–425CrossRefGoogle Scholar
  65. Mendell JR, Shilling C, Leslie ND, Flanigan KM, Al-Dahhak R, Gastier-Foster J, Kneile K, Dunn DM, Duval B, Aoyagi A, Hamil C, Mahmoud M, Roush K, Bird L, Rankin C, Lilly H, Street N, Chandrasekar R, Weiss RB (2012) Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann Neurol 71:304–313. 2012PubMedCrossRefGoogle Scholar
  66. Mestril R, Dillmann WH (1995) Heat shock proteins and protection against myocardial ischemia. J Mol Cell Cardiol 27(1):45–52PubMedCrossRefGoogle Scholar
  67. Morici G, Rappa F, Cappello F, Pace E, Pace A, Mudò G, Crescimanno G, Belluardo N, Bonsignore MR (2016) Lack of dystrophin affects bronchial epithelium in mdx mice. J Cell Physiol 231(10):2218–2223PubMedCrossRefGoogle Scholar
  68. Morimoto RI, Jurivich DA, Kroger PE, Mathur SK, Murphy SP, Nakai A, Sarge AK, Abravaya K, Sistonen LT (1994) Regulation of heat shock gene transcription by a family of heat shock factors. In: Morimoto R, Tissières A, Georgopoulos C (eds) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 417–455Google Scholar
  69. Morley JE, Baumgartner RN, Roubenoff R, Mayer J, Nair KS (2001) Sarcopenia. J Lab Clin Med 137:231–24310PubMedCrossRefGoogle Scholar
  70. Naylor DJ, Hartl FU (2001) Contribution of molecular chaperones to protein folding in the cytoplasm of prokaryotic and eukaryotic cells. Biochem Soc Symp 68:45–68CrossRefGoogle Scholar
  71. O'Gorman P, McMillan DC, McArdle CS (1999) Longitudinal study of weight, appetite, performance status, and inflammation in advanced gastrointestinal cancer. Nutr Can 35(2):127–129CrossRefGoogle Scholar
  72. Osterloh A, Meier Stiegen F, Veit A, Fleischer B, von Bonin A, Breloer M (2004) Lipopolysaccharide- free heat shock protein 60 activates T cells. J Biol Chem 279:47906–47911PubMedCrossRefGoogle Scholar
  73. Pietrangelo T, Puglielli C, Mancinelli R, Beccafico S, Fanò G, Fulle S (2009) Molecular basis of the myogenic profile of aged human skeletal muscle satellite cells during differentiation. Exp Gerontol 44:523–531PubMedCrossRefGoogle Scholar
  74. Piselli P, Vendetti S, Vismara D, Cicconi R, Poccia F, Colizzi V, Delpino A (2000) Different expression of CD44, ICAM-1 and HSP60 on primary tumor and metastases of a human pancreatic carcinoma growing in scid mice. Anticancer Res 20:825–831PubMedGoogle Scholar
  75. Plumier JC, Currie RW (1996) Heat shock-induced myocardial protection against ischemic injury: a role for HSP70? Cell Stress Chaperones 1:13–17PubMedPubMedCentralCrossRefGoogle Scholar
  76. Pockley AG, Fairburn B, Mirza S, Slack LK, Hopkinson K, Muthana M (2007) A non-receptor- mediated mechanism for internalization of molecular chaperones. Methods 43:238–244PubMedPubMedCentralCrossRefGoogle Scholar
  77. Quintana FJ, Cohen IR (2011) The HSP60 immune system network. Trends Immunol 32:89–95PubMedPubMedCentralCrossRefGoogle Scholar
  78. Ranford JC, Henderson B (2002) Chaperonins in disease: mechanisms, models and treatments. Mol Pathol 55:209–213PubMedPubMedCentralCrossRefGoogle Scholar
  79. Rantanen T (2003) Muscle strength, disability and mortality. (2003). Scand J Med Sci Sports 13(1):3–8PubMedCrossRefGoogle Scholar
  80. Rathor R, Sharma P, Suryakumar G, Ganju L (2015) A pharmacological investigation of Hippophae salicifolia (HS) and Hippophae rhamnoides turkestanica (HRT) against multiple stress (C-H-R): an experimental study using rat model. Cell Stress Chaperones 20(5):821–831PubMedPubMedCentralCrossRefGoogle Scholar
  81. Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in Drosophila. Experientia 18:571–573CrossRefGoogle Scholar
  82. Ritossa F (1996) Discovery of the heat shock response. Cell Stress Chaperones 1(2):97–98PubMedPubMedCentralCrossRefGoogle Scholar
  83. Rizzoli R, Reginster JY, Arnal JF, Bautmans I, Beaudart C, Bischoff-Ferrari H, Biver E, Boonen S, Brandi ML, Chines A, Cooper C, Epstein S, Fielding RA, Goodpaster B, Kanis JA, Kaufman JM, Laslop A, Malafarina V, Mañas LR, Mitlak BH, Oreffo RO, Petermans J, Reid K, Rolland Y, Sayer AA, Tsouderos Y, Visser M, Bruyère O (2013) Quality of life in sarcopenia and frailty. Calcif Tissue Int 93(2):101–120PubMedPubMedCentralCrossRefGoogle Scholar
  84. Rosenberg IH (1997) Sarcopenia: origins and clinical relevance. J Nutr 127:990S–991SPubMedCrossRefGoogle Scholar
  85. Santilli V, Bernetti A, Mangone M, Paoloni M (2014) Clinical definition of sarcopenia. Clin Cases Miner Bone Metab 11(3):177–180PubMedPubMedCentralGoogle Scholar
  86. Satyal SH, Chen D, Fox SG, Kramer JM, Morimoto RI (1998) Negative regulation of the heat shock transcriptional response by HSBP1. Genes Dev 12:1962–1974PubMedPubMedCentralCrossRefGoogle Scholar
  87. 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 12:384–392PubMedPubMedCentralCrossRefGoogle Scholar
  88. Shi Y, Mosser DD, Morimoto RI (1998) Molecular chaperones as HSF1-specific transcriptional repressors. Genes Dev 12:654–666PubMedPubMedCentralCrossRefGoogle Scholar
  89. Shin BK, Wang H, Yim AM, Le Naour F, Brichory F, Jang JH, Zhao R, Puravs E, Tra J, Michael CW, Misek DE, Hanash SM (2003) Global profiling of the cell surface proteome of cancer cells uncovers an abundance of proteins with chaperone function. J Biol Chem 278:7607–7616PubMedCrossRefGoogle Scholar
  90. Sigal LH, Williams S, Soltys B, Gupta R (2001) H9724, a monoclonal antibody to Borreliaburg-dorferi’s flagellin, binds to heat shock protein 60 (HSP60) within live neuroblastoma cells: a potential role for HSP60 in peptide hormone signaling and in an autoimmune pathogenesis of the neuropathy of Lyme disease. Cell Mol Neurobiol 21:477–495PubMedCrossRefGoogle Scholar
  91. Soltys BJ, Gupta RS (1997) Cell surface localization of the 60 kDa heat shock chaperonin protein (hsp60) in mammalian cells. Cell Biol Int 21:315–320PubMedCrossRefGoogle Scholar
  92. Tisdale MJ (2002) Cachexia in cancer patients. Nat Rev Cancer 2(11):862–871PubMedCrossRefGoogle Scholar
  93. Tisdale MJ (2010) Cancer cachexia. Curr Opin Gastroenterol 26(2):146–151PubMedCrossRefGoogle Scholar
  94. Tissieres A, Mitchell HK, Tracy UM (1974) Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. J Mol Biol 84(3):389–398PubMedCrossRefGoogle Scholar
  95. Tutar L, Tutar Y (2010) Heat shock proteins; an overview. (2010). Curr Pharm Biotechnol 11(2):216–222PubMedPubMedCentralCrossRefGoogle Scholar
  96. Veereshwarayya V, Kumar P, Rosen KM, Mestril R, Querfurt HW (2016) Differential effects of mitochondrial heat shock protein 60 and related molecular chaperones to prevent intracellular β-amyloid-induced inhibition of complex IV and limit apoptosis. J Biol Chem 281:29468–29478CrossRefGoogle Scholar
  97. Verratti V, Falone S, Doria C, Pietrangelo T, Di Giulio C (2015) Kilimanjaro Abruzzo expedition: effects of high-altitude trekking on anthropometric, cardiovascular and blood biochemical parameters. Sport Sci Health 11(3):271–278PubMedPubMedCentralCrossRefGoogle Scholar
  98. Voellmy R (1994) Transduction of the stress signal and mechanisms of transcriptional regulation of heat shock/stress protein gene expression in higher eukaryotes. Crit Rev Eukaryot Gene Expr 4:357–401PubMedGoogle Scholar
  99. Wang RE (2011) Targeting heat shock proteins 70/90 and proteasome for cancer therapy. Curr Med Chem 18:4250–4264PubMedCrossRefGoogle Scholar
  100. Wiechmann K, Müller H, Konig S, Wielsch N, Svatos A, Jauch J, Werz O (2017) Cell Chem Biol 24(5):614–623PubMedPubMedCentralCrossRefGoogle Scholar
  101. Wu J, Liu T, Rios Z, Mei Q, Lin X, Cao S (2017) Heat shock proteins and cancer. Trends Pharmacol Sci 38:226–256PubMedPubMedCentralCrossRefGoogle Scholar
  102. Zhang G, Liu Z, Ding H, Zhou Y, Doan HA, Sin KWT, Zhu ZJ, Flores R, Wen Y, Gong X, Liu O, Li YP (2017) Tumor induces muscle wasting in mice through releasing extracellular Hsp70 and Hsp90. Nat Commun 8:589PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Richa Rathor
    • 1
    Email author
  • Geetha Suryakumar
    • 1
  • Som Nath Singh
    • 1
  • Bhuvnesh Kumar
    • 1
  1. 1.Cellular Biochemistry GroupDefense Institute of Physiology and Allied SciencesDelhiIndia

Personalised recommendations