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Stem Cell Reviews and Reports

, Volume 15, Issue 5, pp 637–651 | Cite as

Heat Shock Proteins and their Protective Roles in Stem Cell Biology

  • Pravin ShendeEmail author
  • Sayali Bhandarkar
  • Bala Prabhakar
Article
  • 369 Downloads

Abstract

Stem cells (SCs) are discovered long back but the idea that SCs possess therapeutic potential came up just a few decades back. In a past decade stem cell therapy is highly emerged and displayed tremendous potential for the treatment of a wide range of diseases and disorders such as blindness and vision impairment, type I diabetes, infertility, HIV, etc. SCs are very susceptible to destruction after transplantation into the host because of the inability to sustain elevated stress conditions inside the damaged tissue/organ. Heat shock proteins (HSPs) are molecular chaperones/stress proteins expressed in response to stress (elevated temperature, harmful chemicals, ischemia, viruses, etc) inside a living cell. HSPs protect the cell from damage by assisting in the proper folding of cellular proteins. This review briefly summarises different types of HSPs, their classification, cellular functions as well as the role of HSPs in regulating SC self-renewal and survival in the transplanted host. Applications of HSP modulated SCs in regenerative medicine and for the treatment of ischemic heart disease, myocardial infarction (MI), osteoarthritis, ischemic stroke, spinocerebellar ataxia type 3 (SCA3), leukemia, hepatic ischemia-reperfusion injury, Graft-versus-host disease (GVHD) and Parkinson’s disease (PD) are discussed. In order to provide potential insights in understanding molecular mechanisms related to SCs in vertebrates, correlations between HSPs and SCs in cnidarians and planarians are also reviewed. There is a need to advance research in order to validate the use of HSPs for SC therapy and establish effective treatment strategies.

Keywords

Heat shock proteins Stem cells Stress proteins Molecular chaperones Self-renewal 

Abbreviations

SCs

Stem cells

HSPs

Heat shock proteins

MI

Myocardial infarction

SCA3

Spinocerebellar ataxia type 3

GVHD

Graft-versus-host disease

PD

Parkinson’s disease

ESCs

Embryonic stem cells

ASCs

Adult stem cells

hMSCs

Human mesenchymal stem cells

HSFs

Heat shock factors

mESCS

Mouse embryonic stem cells

NANOG

Homeobox protein NANOG

STAT3

Signal transducer and activator of transcription 3

OCT4

Octamer-binding transcription factor 4

SOX2

Sex-determining region Y-box 2

MSCs

Mesenchymal stem cells

NSCs

Neural stem cells

CSCs

Cancer stem cells

GRP78

Glucose-regulated protein

IGF

Insulin-like growth factor

FGF-2

Fibroblast growth factors

VEGF

Vascular endothelial growth factor

HSCs

Hematopoietic stem cells

ROS

Reactive oxygen species

LIF

Leukemia inhibitory factor

17-AAG

17-N-Allylamino-17-demethoxygeldanamycin

PDX-1

Insulin promoter factor 1

SN

Substantia nigra

CML

Chronic myeloid leukemia

IPI-504

Retaspimycin hydrochloride

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

12015_2019_9903_MOESM1_ESM.docx (1.6 mb)
ESM 1 (DOCX 1629 kb)

References

  1. 1.
    Romito A, Cobellis G. Pluripotent stem cells: Current understanding and future directions. Stem Cells International [Internet] 2016 [cited 2019 May 31];2016:9451492. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26798367 (Accessed on 2019 May 31).
  2. 2.
    Fan G-C. Role of Heat Shock proteins in stem cell behavior [Internet]. In: Progress in Molecular Biology and Translational Science. 2012 [cited 2019 Feb 24]. p. 305–322. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22917237 (Accessed on 2019 February 24).
  3. 3.
    Gao F, Hu X, Xie X, et al. Heat shock protein 90 protects rat mesenchymal stem cells against hypoxia and serum deprivation-induced apoptosis via the PI3K/Akt and ERK1/2 pathways. Journal of Zhejiang University. Science. B [Internet] 2010;11(8):608–617. Available from: http://www.springerlink.com/index/10.1631/jzus.B1001007 (Accessed on 2019 February 6).
  4. 4.
    Whitley D, Goldberg SP, Jordan WD. Heat shock proteins: A review of the molecular chaperones. Journal of Vascular Surgery [Internet] 1999 [cited 2019 Jan 18];29(4):748–751. Available from: https://www.sciencedirect.com/science/article/pii/S0741521499703290 (Accessed on 2019 January 18).
  5. 5.
    Doberentz E, Genneper L, Wagner R, Madea B. Expression times for hsp27 and hsp70 as an indicator of thermal stress during death due to fire. International Journal of Legal Medicine [Internet] 2017 [cited 2019 Jan 18];131(6):1707–1718. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28233103 (Accessed on 2019 January 18).
  6. 6.
    Candido EPM. Heat Shock proteins. Encycl Genet [Internet] 2001 [cited 2019 Jan 3];914–915. Available from: https://www.sciencedirect.com/science/article/pii/B0122270800005887 (Accessed on 2019 January 3).
  7. 7.
    Lindquist S, Craig EA. The Heat-Shock proteins. Annual Review of Genetics [Internet] 1988 [cited 2019 Jan 20];22(1):631–677. Available from: http://www.annualreviews.org/doi/10.1146/annurev.ge.22.120188.003215 (Accessed on 2019 January 20).
  8. 8.
    Richter K, Haslbeck M, Buchner J. The Heat Shock response: Life on the verge of death. Molecular Cell [Internet] 2010 [cited 2019 Jan 19];40(2):253–266. Available from: https://www.sciencedirect.com/science/article/pii/S1097276510007823 (Accessed on 2019 January 19).
  9. 9.
    Guo M, Liu J-H, Ma X, Luo D-X, Gong Z-H, Lu M-H. The plant Heat stress transcription factors (HSFs): Structure, regulation, and function in response to abiotic stresses. Frontiers in Plant Science [Internet] 2016 [cited 2019 Mar 15];7:114. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26904076 (Accessed on 2019 March 15).
  10. 10.
    Saju JM, Hossain MS, Liew WC, et al. Heat Shock factor 5 is conserved in vertebrates and essential for spermatogenesis in zebrafish. SSRN Electronic Journal [Internet] 2018 [cited 2019 Mar 15]; Available from: https://www.ssrn.com/abstract=3155586 (Accessed on 2019 March 15).
  11. 11.
    Åkerfelt M, Morimoto RI, Sistonen L. Heat shock factors: Integrators of cell stress, development and lifespan. Nature Reviews. Molecular Cell Biology [Internet] 2010 [cited 2019 Jan 20];11(8):545–555. Available from: http://www.nature.com/articles/nrm2938 (Accessed on 2019 January 20).
  12. 12.
    Soo ET-L, Ng Y-K, Bay B-H, Yip GW-C. Heat Shock proteins and neurodegenerative disorders. Scientific World Journal [Internet] 2008 [cited 2019 Feb 24];8:270–274. Available from: http://www.hindawi.com/journals/tswj/2008/973631/abs/ (Accessed on 2019 February 24).
  13. 13.
    Jee H. Size dependent classification of heat shock proteins: A mini-review. J Exerc Rehabil [Internet] 2016 [cited 2019 Jun 2];12(4):255–259. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27656620 (Accessed on 2019 June 2).
  14. 14.
    K D, K R, DK D. Heat Shock Proteins (Hsp): Classifications and its involvement in health and disease. J Pharm Care Heal Syst [Internet] 2017 [cited 2019 Jun 2];4(2):1–3. Available from: https://www.omicsgroup.org/journals/heat-shock-proteins-hsp-classifications-and-its-involvement-in-healthanddisease-2376-0419-1000175.php?aid=88512 (Accessed on 2019 June 2).
  15. 15.
    Banfi G, Dolci A, Verna R, Corsi MM. Exercise raises serum heat-shock protein 70 (Hsp70) levels. Clinical Chemistry and Laboratory Medicine [Internet] 2004 [cited 2019 Jun 4];42(12):1445–1446. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15576310 (Accessed on 2019 June 4).
  16. 16.
    Zuo D, Subjeck J, Wang X-Y. Unfolding the role of large Heat Shock proteins: New insights and therapeutic implications. Frontiers in Immunology [Internet] 2016 [cited 2019 Jun 4];7:75. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26973652(Accessed on 2019 June 4).
  17. 17.
    Shende P, Gupta H, Gaud RS. Cytotherapy using stromal cells: Current and advance multi-treatment approaches. Biomed Pharmacother [Internet] 2018;97(September 2017):38–44. Available from: doi: https://doi.org/10.1016/j.biopha.2017.10.127 (Accessed on 24 March 2019).
  18. 18.
    Chambers I, Colby D, Robertson M, et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell [Internet] 2003 [cited 2019 Jan 22];113(5):643–655. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0092867403003921 (Accessed on 2019 January 22).
  19. 19.
    Mitsui K, Tokuzawa Y, Itoh H, et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell [Internet] 2003 [cited 2019 Feb 24];113(5):631–642. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12787504 (Accessed on 2019 March 18).
  20. 20.
    Raz R, Lee C-K, Cannizzaro LA, d’Eustachio P, Levy DE. Essential role of STAT3 for embryonic stem cell pluripotency. Proceedings of the National Academy of Sciences [Internet] 1999 [cited 2019 Jan 22];96(6):2846–2851. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.96.6.2846 (Accessed on 2019 January 22).
  21. 21.
    Niwa H, Burdon T, Chambers I, Smith A. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes & Development [Internet] 1998 [cited 2019 Jan 22];12(13):2048–2060. Available from: http://www.genesdev.org/cgi/doi/10.1101/gad.12.13.2048 (Accessed on 2019 January 22).
  22. 22.
    Bensaude O, Morange M. Spontaneous high expression of heat-shock proteins in mouse embryonal carcinoma cells and ectoderm from day 8 mouse embryo. The EMBO Journal [Internet] 1983 [cited 2019 Jun 4];2(2):173–177. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11894922 (Accessed on 2019 June 4).
  23. 23.
    Lathia JD, Venere M, Rao MS, Rich JN. Seeing is believing: Are cancer stem cells the loch ness monster of tumor biology? Stem Cell Reviews [Internet] 2011 [cited 2019 Jun 4];7(2):227–237. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20957452 (Accessed on 2019 June 4).
  24. 24.
    Luo S, Mao C, Lee B, Lee AS. GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Molecular and Cellular Biology [Internet] 2006 cited 2019 Jun 4];26(15):5688–5697. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16847323 (Accessed on 2019 June 4).
  25. 25.
    Baharvand H, Fathi A, Gourabi H, Mollamohammadi S, Salekdeh GH. Identification of mouse embryonic stem cell-associated proteins. Journal of Proteome Research [Internet] 2008 [cited 2019 Jun 4];7(1):412–423. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18047272 (Accessed on 2019 June 4).
  26. 26.
    Battersby A, Jones RD, Lilley KS, et al. Comparative proteomic analysis reveals differential expression of Hsp25 following the directed differentiation of mouse embryonic stem cells. Biochim Biophys Acta - Mol Cell Res [Internet] 2007 [cited 2019 Jun 4];1773(2):147–156. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17030443 (Accessed on 2019 June 4).
  27. 27.
    DeLany JP, Floyd ZE, Zvonic S, et al. Proteomic analysis of primary cultures of human adipose-derived stem cells. Molecular & Cellular Proteomics [Internet] 2005 [cited 2019 Jun 4];4(6):731–740. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15753122 (Accessed on 2019 June 4).
  28. 28.
    Suzuki K. Role of Interleukin-1 in acute inflammation and graft death after cell transplantation to the heart. Circulation [Internet] 2004 [cited 2019 Feb 3];110(11_suppl_1):II-219-II-224. Available from: http://circ.ahajournals.org/cgi/doi/10.1161/01.CIR.0000138388.55416.06 (Accessed on 2019 February 3).
  29. 29.
    Müller-Ehmsen J, Whittaker P, Kloner RA, et al. Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. Journal of Molecular and Cellular Cardiology [Internet] 2002 [cited 2019 Feb 3];34(2):107–116. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0022282801914919 (Accessed on 2019 February 3).
  30. 30.
    Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation [Internet] 2002 [cited 2019 Feb 3];105(1):93–98. Available from: https://www.ahajournals.org/doi/10.1161/hc0102.101442 (Accessed on 2019 February 3).
  31. 31.
    Freyman T, Polin G, Osman H, et al. A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction. European Heart Journal [Internet] 2006 [cited 2019 Feb 3];27(9):1114–1122. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16510464 (Accessed on 2019 February 3).
  32. 32.
    Jäättelä M. Heat shock proteins as cellular lifeguards. Annals of Medicine [Internet] 1999 [cited 2019 Feb 3];31(4):261–271. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10480757 (Accessed on 2019 February 3).
  33. 33.
    Prinsloo E, Setati MM, Longshaw VM, Blatch GL. Chaperoning stem cells: A role for heat shock proteins in the modulation of stem cell self-renewal and differentiation? BioEssays 2009;31(4):370–377. (Accessed on 2019 April 3).Google Scholar
  34. 34.
    Čížková D, Rosocha J, Vanický I, Radonák J, Gálik J, Čížek M. Induction of mesenchymal stem cells leads to HSP72 synthesis and higher resistance to oxidative stress. Neurochemical Research [Internet] 2006 [cited 2019 Feb 3];31(8):1011–1020. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16865557 (Accessed on 2019 February 3).
  35. 35.
    Chang W, Song B-W, Lim S, et al. Mesenchymal stem cells pretreated with delivered Hph-1-Hsp70 protein are protected from hypoxia-mediated cell death and rescue heart functions from myocardial injury. Stem Cells [Internet] 2009 [cited 2019 Feb 17];27(9):2283–2292. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19544472 (Accessed on 2019 February 17).
  36. 36.
    Wang X, Zhao T, Huang W, et al. Hsp20-engineered mesenchymal stem cells are resistant to oxidative stress via enhanced activation of Akt and increased secretion of growth factors. Stem Cells [Internet] 2009 [cited 2019 Feb 17];27(12):N/A-N/A. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19816949 (Accessed on 2019 February 17).
  37. 37.
    Son GH, Geum D, Chung S, et al. A protective role of 27-kDa heat shock protein in glucocorticoid-evoked apoptotic cell death of hippocampal progenitor cells. Biochemical and Biophysical Research Communications [Internet] 2005 [cited 2019 Feb 17];338(4):1751–1758. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0006291X05024460 (Accessed on 2019 February 17).
  38. 38.
    Wu W, Welsh MJ. Expression of the 25-kDa heat-shock protein (HSP27) correlates withresistance to the toxicity of cadmium chloride, mercuric chloride, cis-platinum(II)-diammine dichloride, or sodium arsenite in mouse embryonic stem cells transfected with sense or antisense HSP27 cDNA. Toxicology and Applied Pharmacology [Internet] 1996 [cited 2019 Feb 24];141(1):330–339. Available from: https://www.sciencedirect.com/science/article/pii/S0041008X96800391 (Accessed on 2019 February 24).
  39. 39.
    Stolzing A, Sethe S, Scutt AM. Stressed stem cells: Temperature response in aged mesenchymal stem cells. Stem Cells and Development [Internet] 2006 [cited 2019 Mar 16];15(4):478–487. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16978051 (Accessed on 2019 March 16).
  40. 40.
    Yu, S. J., Tajiri, N., Franzese, N., et al. (2013). Stem cell-like dog placenta cells afford neuroprotection against ischemic stroke model via heat shock protein upregulation. PLoS One, 8(9), 1–10 Accessed on 2019 April 17.Google Scholar
  41. 41.
    Tai-Nagara I, Matsuoka S, Ariga H, Suda T. Mortalin and DJ-1 coordinately regulate hematopoietic stem cell function through the control of oxidative stress. Blood 2014;123(1):41–50. (Accessed on 2019 April 12).Google Scholar
  42. 42.
    Lin T, Chao C, Saito S, et al. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nature Cell Biology 2005;7(2):165–171. (Accessed on 2019 April 13).Google Scholar
  43. 43.
    Longshaw VM, Baxter M, Prewitz M, Blatch GL. Knockdown of the co-chaperone hop promotes extranuclear accumulation of Stat3 in mouse embryonic stem cells. European Journal of Cell Biology 2009;88(3):153–166. (Accessed on 2019 April 15).Google Scholar
  44. 44.
    Duffy, D. J., Millane, R. C., & Frank, U. (2012). A heat shock protein and Wnt signaling crosstalk during axial patterning and stem cell proliferation. Developmental Biology, 362(2), 271–281 Accessed on 2019 April 16.PubMedGoogle Scholar
  45. 45.
    Kim, H. W., Wen, Z., Modi, R. M., et al. (2013). Heat shock improves Sca-1 + stem cell survival and directs ischemic cardiomyocytes toward a Prosurvival phenotype via Exosomal transfer: A critical role for HSF1/miR-34a/HSP70 pathway. Stem Cells, 32(2), 462–472 Accessed on 2019 April 16.Google Scholar
  46. 46.
    Yu SJ, Tajiri N, Franzese N, et al. Stem cell-like dog placenta cells afford neuroprotection against ischemic stroke model via Heat Shock protein upregulation. PLoS One 2013;8(9):1–10. (Accessed on 2019 April 17).Google Scholar
  47. 47.
    Serena E, Figallo E, Tandon N, et al. Electrical stimulation of human embryonic stem cells: Cardiac differentiation and the generation of reactive oxygen species. Experimental Cell Research 2009 [cited 2019 Mar 11], 315(20), 3611–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19720058 (Accessed on 2019 March 11).
  48. 48.
    Koga, T., Shiraki, N., Yano, S., et al. (2017). Mild electrical stimulation with heat shock guides differentiation of embryonic stem cells into Pdx1-expressing cells within the definitive endoderm. BMC Biotechnology, 17(1), 1–7 Accessed on 2019 April 18.Google Scholar
  49. 49.
    McGinley, L., McMahon, J., Strappe, P., et al. (2011). Lentiviral vector mediated modification of mesenchymal stem cells & enhanced survival in an in vitro model of ischaemia. Stem Cell Research & Therapy, 2(2), 12 Available from: http://stemcellres.com/content/2/2/12 (Accessed on 2019 April 20).Google Scholar
  50. 50.
    Shende P, Rodrigues B, Gaud RS. Transplantation and alternatives to treat autoimmune diseases [Internet]. 2018 [cited 2019 Mar 18]. p. 59–72. Available from: http://link.springer.com/10.1007/5584_2018_177 (Accessed on 2019 March 18).
  51. 51.
    Goral, J., Shenoy, S., Mohanakumar, T., & Clancy, J. (2002). Antibodies to 70 kD and 90 kD heat shock proteins are associated with graft-versus-host disease in peripheral blood stem cell transplant recipients. Clinical and Experimental Immunology, 127(3), 553–559 (Accessed on 2019 April 21).PubMedPubMedCentralGoogle Scholar
  52. 52.
    Zhang, M., Lu, Z., Li, T., et al. (2017). Human umbilical cord mesenchymal stem cells protect against SCA3 by modulating the level of 70 kD heat shock protein. Cellular and Molecular Neurobiology, 38(3), 641–655 (Accessed on 2019 April 22).PubMedGoogle Scholar
  53. 53.
    Grinchuk, T. M., Zenin, V. V., Kovaleva, Z. V., et al. (2012). Heat shock induces apoptosis in human embryonic stem cells but a premature senescence phenotype in their differentiated progeny. Cell Cycle, 11(17), 3260–3269.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Park, J. A., Kim, Y. E., Seok, H. J., Park, W. Y., Kwon, H. J., & Lee, Y. (2011). Differentiation and upregulation of heat shock protein 70 induced by a subset of histone deacetylase inhibitors in mouse and human embryonic stem cells. BMB Reports, 44(3), 176–181.PubMedGoogle Scholar
  55. 55.
    Nolan, K. D., Kaur, J., & Isaacs, J. S. (2017). Secreted heat shock protein 90 promotes prostate cancer stem cell heterogeneity. Oncotarget, 8(12), 19323–19341 Available from: http://www.oncotarget.com/fulltext/14252.PubMedGoogle Scholar
  56. 56.
    Duffy, D. J., Millane, R. C., & Frank, U. (2012). A heat shock protein and Wnt signaling crosstalk during axial patterning and stem cell proliferation. Developmental Biology, 362(2), 271–281.PubMedGoogle Scholar
  57. 57.
    Isolani, M. E., Conte, M., Deri, P., & Batistoni, R. (2012). Stem cell protection mechanisms in planarians: The role of some heat shock genes. The International Journal of Developmental Biology, 56(1–3), 127–133.PubMedGoogle Scholar
  58. 58.
    Wu, K. H., Mo, X. M., Han, Z. C., & Zhou, B. (2011). Stem cell engraftment and survival in the ischemic heart. The Annals of Thoracic Surgery, 92(5), 1917–1925 Available from: https://linkinghub.elsevier.com/retrieve/pii/S0003497511017346.PubMedGoogle Scholar
  59. 59.
    Kim, H. W., Wen, Z., Modi, R. M., et al. (2013). Heat shock improves Sca-1 + stem cell survival and directs ischemic cardiomyocytes toward a Prosurvival phenotype via Exosomal transfer: A critical role for HSF1/miR-34a/HSP70 pathway. Stem Cells, 32(2), 462–472.Google Scholar
  60. 60.
    Feng, Y., Huang, W., Meng, W., et al. (2014). Heat shock improves Sca-1 + stem cell survival and directs ischemic cardiomyocytes toward a prosurvival phenotype via exosomal transfer: A critical role for HSF1/miR-34a/HSP70 pathway. Stem Cells, 32(2), 462–472 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24123326.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Yu, S. J., Tajiri, N., Franzese, N., et al. (2013). Stem cell-like dog placenta cells afford neuroprotection against ischemic stroke model via heat shock protein upregulation. PLoS One, 8(9), 1–10.Google Scholar
  62. 62.
    Tawfeeq, A. T., Mahmood, N. A.-A., & Abd-Alghni, Z. S. (2019). Starvation contributes to elevated levels of heat shock proteins and cancer stem cell markers in an esophageal cancer cell line. Biomedical Research, 29(21), 3815–3823.Google Scholar
  63. 63.
    Chen, J., Li, C., & Wang, S. (2014). Periodic heat shock accelerated the Chondrogenic differentiation of human mesenchymal stem cells in pellet culture. PLoS One, 9(3).Google Scholar
  64. 64.
    Yamada, M., Tanemura, K., Okada, S., et al. (2006). Electrical stimulation modulates fate determination of differentiating embryonic stem cells. Stem Cells, 25(3), 562–570 Available from: http://www.ncbi.nlm.nih.gov/pubmed/17110622.PubMedGoogle Scholar
  65. 65.
    Serena, E., Figallo, E., Tandon, N., Cannizzaro, C., Gerecht, S., Elvassore, N., & Vunjak-Novakovic, G. (2009). Electrical stimulation of human embryonic stem cells: Cardiac differentiation and the generation of reactive oxygen species. Experimental Cell Research, 315(20), 3611–3619 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19720058.PubMedPubMedCentralGoogle Scholar
  66. 66.
    Koga, T., Shiraki, N., Yano, S., et al. (2017). Mild electrical stimulation with heat shock guides differentiation of embryonic stem cells into Pdx1-expressing cells within the definitive endoderm. BMC Biotechnology, 17(1), 1–7.Google Scholar
  67. 67.
    McGinley, L. M., McMahon, J., Stocca, A., et al. (2013). Mesenchymal stem cell survival in the infarcted heart is enhanced by lentivirus vector-mediated heat shock protein 27 expression. Human Gene Therapy, 24(10), 840–851 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23987185.PubMedPubMedCentralGoogle Scholar
  68. 68.
    McGinley, L., McMahon, J., Strappe, P., Barry, F., Murphy, M., O'Toole, D., & O'Brien, T. (2011). Lentiviral vector mediated modification of mesenchymal stem cells & enhanced survival in an in vitro model of ischaemia. Stem Cell Research & Therapy, 2(2), 12 Available from: http://stemcellres.com/content/2/2/12.Google Scholar
  69. 69.
    Shende, P., Rodrigues, B., & Gaud, R. S. (2018). Transplantation and alternatives to treat autoimmune diseases. Advances in Experimental Medicine and Biology, 1089, 59–72.  https://doi.org/10.1007/5584_2018_177.PubMedGoogle Scholar
  70. 70.
    Goral, J., Shenoy, S., Mohanakumar, T., & Clancy, J. (2002). Antibodies to 70 kD and 90 kD heat shock proteins are associated with graft-versus-host disease in peripheral blood stem cell transplant recipients. Clinical and Experimental Immunology, 127(3), 553–559.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Qiao, P. F., Yao, L., Zhang, X. C., Li, G. D., & Wu, D. Q. (2015). Heat shock pretreatment improves stem cell repair following ischemia-reperfusion injury via autophagy. World Journal of Gastroenterology, 21(45), 12822–12834.PubMedPubMedCentralGoogle Scholar
  72. 72.
    Zhao, C., Li, H., Zhao, X. J., Liu, Z. X., Zhou, P., Liu, Y., & Feng, M. J. (2016). Heat shock protein 60 affects behavioral improvement in a rat model of Parkinson’s disease grafted with human umbilical cord mesenchymal stem cell-derived dopaminergic-like neurons. Neurochemical Research, 41(6), 1238–1249.PubMedGoogle Scholar
  73. 73.
    Peng, C., Li, D., & Li, S. (2007). Heat shock protein 90: A potential therapeutic target in leukemic progenitor and stem cells harboring mutant BCR-ABL resistant to kinase inhibitors. Cell Cycle, 6(18), 2227–2231.PubMedGoogle Scholar
  74. 74.
    Read, M., Goodrich, A., Li, S., et al. (2007). Inhibition of heat shock protein 90 prolongs survival of mice with BCR-ABL-T315I-induced leukemia and suppresses leukemic stem cells. Blood, 110(2), 678–685.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Shaik, S., Hayes, D., Gimble, J., & Devireddy, R. (2017). Inducing heat shock proteins enhances the Stemness of frozen–thawed adipose tissue-derived stem cells. Stem Cells and Development, 26(8), 608–616.  https://doi.org/10.1089/scd.2016.0289.PubMedPubMedCentralGoogle Scholar
  76. 76.
    Zhang, M., Lu, Z., Li, T., et al. (2017). Human umbilical cord mesenchymal stem cells protect against SCA3 by modulating the level of 70 kD heat shock protein. Cellular and Molecular Neurobiology, 38(3), 641–655.PubMedGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Shobhaben Pratapbhai Patel School of Pharmacy and Technology ManagementSVKM’s NMIMSMumbaiIndia

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