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Chaperone-Like Proteins in Inflammation and Immunomodulation: Examples of Resistin and PPIases

  • Saurabh Pandey
  • Javeed Ahmad
  • Nasreen Zafar Ehtesham
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 16)

Abstract

Hsp and other small proteins that function as an accessory chaperones interact with the cellular signaling network. They come up as an immediate response to stress when cells face the challenge of its own programmed death response. Chaperokines, with their inflammation and immune modulatory potential, try to strike the balance between recovery to normalcy and programmed death. Various disease pathways, environmental stresses, toxins and infections are the challenges that mount fatal stress. Resistin, an adipokine in murine model, small macrophage secreted protein in human and PPIases of Mycobacterium tuberculosis are the potential chaperokines. Though according to classical definition they do not fall under the category of HSP having α-crystalline domain, they function as small chaperone and are part of biological diversity where evolutionary conserved and adapted survival mechanisms work in parallel to protect and sustain life.

Keywords

Chaperokine Heat shock protein Immunomodulation Inflammation PPIase Resistin 

Abbreviations

ATP

Adenosine triphosphate

CAP-1

Adenylyl cyclase-associated protein 1

Cyp

Cyclophilin

E. coli

Escherichia coli

ER

Endoplasmic reticulum

FKBP

FK506 binding protein

FoxP3

Forkhead Box P3

hRes

Human Resistin

HSP

Heat shock protein family

Hsp

Heat shock proteins

IL

Interleukin

IRF-1

Interferon regulatory factor 1

M.tb

Mycobacterium tuberculosis

MIP

Macrophage infectivity potentiator

NFAT

Nuclear factor of activated T cells

NFκB

Nuclear factor kappa B

PIN1

Peptidyl-prolyl cis-trans isomerase NIMA-interacting 1

PPIases

Peptidyl-prolyl cis/trans isomerases

SDS

Sodium dodecyl sulfate

SH3

Src homology 3

TLR

Toll-like receptors

TNF

Tumor necrosis factor

Treg

Regulatory T cells

UPR

Unfolded protein response

WD40

WD (Trp-Asp) or beta-transducin repeat motif

Notes

Acknowledgements

NZE would like to thank Centre of Excellence research grant (BT/PR12817/COE/34/23/2015) from the Department of Biotechnology, Ministry of Science and Technology (DBT), Government of India and research grant (No.5/9/1019/2011-RHN) from ICMR, Ministry of Health and Family welfare, Government of India for financial support.

References

  1. Arora K, Gwinn WM, Bower MA, Watson A, Okwumabua I, MacDonald HR, Bukrinsky MI, Constant SL (2005) Extracellular cyclophilins contribute to the regulation of inflammatory responses. J Immunol 175:517CrossRefGoogle Scholar
  2. Aruna B, Ghosh S, Singh AK, Mande SC, Srinivas V, Chauhan R, Ehtesham NZ (2003) Human recombinant resistin protein displays a tendency to aggregate by forming intermolecular disulfide linkages. Biochemistry 42:10554–10559CrossRefGoogle Scholar
  3. Aruna B, Islam A, Ghosh S, Singh AK, Vijayalakshmi M, Ahmad F, Ehtesham NZ (2008) Biophysical analyses of human resistin: oligomer formation suggests novel biological function. Biochemistry 47:12457–12466CrossRefGoogle Scholar
  4. Asquith KL, Baleato RM, McLaughlin EA, Nixon B, Aitken RJ (2004) Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci 117:3645–3657CrossRefGoogle Scholar
  5. Basha E, O’Neill H, Vierling E (2012) Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37:106–117CrossRefGoogle Scholar
  6. Bhuwan M, Arora N, Sharma A, Khubaib M, Pandey S, Chaudhuri TK, Hasnain SE, Ehtesham NZ (2016) Interaction of Mycobacterium tuberculosis virulence factor RipA with chaperone MoxR1 is required for transport through the TAT secretion system. MBio 7:1–12CrossRefGoogle Scholar
  7. Blackburn EA, Walkinshaw MD (2011) Targeting FKBP isoforms with small-molecule ligands. Curr Opin Pharmacol 11:365–371CrossRefGoogle Scholar
  8. D’Andrea LD, Regan L (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28:655–662CrossRefGoogle Scholar
  9. Dalamaga M, Karmaniolas K, Papadavid E, Pelekanos N, Sotiropoulos G, Lekka A (2013) Hyperresistinemia is associated with postmenopausal breast cancer. Menopause 20:845–851CrossRefGoogle Scholar
  10. Danese E, Montagnana M, Minicozzi AM, Bonafini S, Ruzzenente O, Gelati M, De Manzoni G, Lippi G, Guidi GC (2012) The role of resistin in colorectal cancer. Clin Chim Acta 413:760–764CrossRefGoogle Scholar
  11. Ehtesham NZ, Nasiruddin M, Alvi A, Kumar BK, Ahmed N, Peri S, Murthy KJR, Hasnain SE (2011) Treatment end point determinants for pulmonary tuberculosis: human resistin as a surrogate biomarker. Tuberculosis 91:293–299CrossRefGoogle Scholar
  12. Esnault S, Braun RK, Shen ZJ, Xiang Z, Heninger E, Love RB, Sandor M, Malter JS (2007) Pin1 modulates the type 1 immune response. PLoS One 2:e226CrossRefGoogle Scholar
  13. Fischer G, Bang H, Ludwig B, Mann K, Hacker J (1992) Mip protein of Legionella pneumophila exhibits peptidyl-prolyl-cis/trans isomerase (PPlase) activity. Mol Microbiol 6:1375–1383CrossRefGoogle Scholar
  14. Freeman BC, Toft DO, Morimoto RI (1996) Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science 274:1718–1720CrossRefGoogle Scholar
  15. Ghosh S, Singh AK, Aruna B, Mukhopadhyay S, Ehtesham NZ (2003) The genomic organization of mouse resistin reveals major differences from the human resistin: functional implications. Gene 305:27–34CrossRefGoogle Scholar
  16. Gothel SF, Marahiel MA (1999) Peptidyl-prolylcis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol Life Sci 55:423–436CrossRefGoogle Scholar
  17. Harrison R, Stein RL (1992) Mechanistic studies of enzymatic and nonenzymatic prolyl cis-trans isomerization. J Am Chem Soc 114:3464–3471CrossRefGoogle Scholar
  18. Henderson B (2010) Integrating the cell stress response: a new view of molecular chaperones as immunological and physiological homeostatic regulators. Cell Biochem Funct 28:1–14CrossRefGoogle Scholar
  19. Hishiya A, Takayama S (2008) Molecular chaperones as regulators of cell death. Oncogene 27:6489–6506CrossRefGoogle Scholar
  20. Hlavna M, Kohut L, Lipkova J, Bienertova-Vasku J, Dostalova Z, Chovanec J, Vasku A (2011) Relationship of resistin levels with endometrial cancer risk. Neoplasma 58:124–128CrossRefGoogle Scholar
  21. Ideno A, Furutani M, Iba Y, Kurosawa Y, Maruyama T (2002) FK506 binding protein from the hyper-thermophilic archaeon Pyrococcus horikoshii suppresses the aggregation of proteins in Escherichia coli. Appl Environ Microbiol 68:464–469CrossRefGoogle Scholar
  22. Kaser S, Kaser A, Sandhofer A, Ebenbichler CF, Tilg H, Patsch JR (2003) Resistin messenger-RNA expression is increased by proinflammatory cytokines in vitro. Biochem Biophys Res Commun 309:286–290CrossRefGoogle Scholar
  23. Kim KH, Lee K, Moon YS, Sul HS (2001) A cysteine-rich adipose tissue-specific secretory factor inhibits adipocyte differentiation. J Biol Chem 276:11252–11256CrossRefGoogle Scholar
  24. Kramer G, Patzelt H, Rauch T, Kurz TA, Vorderwülbecke S, Bukau B, Deuerling E (2004) Trigger factor peptidyl-prolylcis/trans isomerase activity is not essential for the folding of cytosolic proteins in Escherichia coli. J Biol Chem 279:14165–14170CrossRefGoogle Scholar
  25. Kumar A, Alam A, Rani M, Ehtesham NZ, Hasnain SE (2017) Biofilms: survival and defense strategy for pathogens. Int J Med Microbiol 307:481–489CrossRefGoogle Scholar
  26. Kurek I, Pirkl F, Fischer E, Buchner J, Breiman A (2002) Wheat FKBP73 functions in vitro as a molecular chaperone independently of its peptidylprolylcis-trans isomerase activity. Planta 215:119–126CrossRefGoogle Scholar
  27. Lee JH, Chan JL, Yiannakouris N, Kontogianni M, Estrada E, Seip R, Orlova C, Mantzoros CS (2003) Circulating resistin levels are not associated with obesity or insulin resistance in humans and are not regulated by fasting or leptin administration: cross-sectional and interventional studies in normal, insulin-resistant, and diabetic subjects. J Clin Endocrinol Metab 88:4848–4856CrossRefGoogle Scholar
  28. Lehrke M, Reilly MP, Millington SC, Iqbal N, Rader DJ, Lazar MA (2004) An inflammatory cascade leading to hyperresistinemia in humans. PLoS Med 1:161–168CrossRefGoogle Scholar
  29. Lin C-H, Li H-Y, Lee Y-C, Calkins MJ, Lee K-H, Yang C-N, Lu P-J (2015) Landscape of Pin1 in the cell cycle. Exp Biol Med 240:403–408CrossRefGoogle Scholar
  30. Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–677CrossRefGoogle Scholar
  31. Liu J, Farmer JD, Lane WS, Friedman J, Weissman I, Schreiber SL (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66:807–815CrossRefGoogle Scholar
  32. Mayr C, Richter K, Lilie H, Buchner J (2000) Cpr6 and Cpr7, two closely related Hsp90-associated immunophilins from Saccharomyces cerevisiae, differ in their functional properties. J Biol Chem 275:34140–34146CrossRefGoogle Scholar
  33. Mchaourab HS, Godar JA, Stewart PL (2009) Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins. Biochemistry 48:3828–3837CrossRefGoogle Scholar
  34. McNaughton L, Li Z, Van Roey P, Hanes SD, LeMaster DM (2010) Restricted domain mobility in the Candida albicans Ess1 prolylisomerase. Biochim Biophys Acta 1804:1537–1541CrossRefGoogle Scholar
  35. Nakajima TE, Yamada Y, Hamano T, Furuta K, Gotoda T, Katai H, Kato K, Hamaguchi T, Shimada Y (2009) Adipocytokine levels in gastric cancer patients: resistin and visfatin as biomarkers of gastric cancer. J Gastroenterol 44:685–690CrossRefGoogle Scholar
  36. Nakajima TE, Yamada Y, Hamano T, Furuta K, Matsuda T, Fujita S, Kato K, Hamaguchi T, Shimada Y (2010a) Adipocytokines as new promising markers of colorectal tumors: adiponectin for colorectal adenoma, and resistin and visfatin for colorectal cancer. Cancer Sci 101:1286–1291CrossRefGoogle Scholar
  37. Naoumov NV (2014) Cyclophilin inhibition as potential therapy for liver diseases. J Hepatol 61:1166–1174CrossRefGoogle Scholar
  38. Pandey S, Sharma A, Tripathi D, Kumar A, Khubaib M, Bhuwan M, Chaudhuri TK, Hasnain SE, Ehtesham NZ (2016) Mycobacterium tuberculosis peptidyl-prolyl isomerases also exhibit chaperone like activity in-vitro and in-vivo. PLoS One 11:e0150288CrossRefGoogle Scholar
  39. Pandey S, Tripathi D, Khubaib M, Kumar A, Shekh AJ, Gaddam S, Ehtesham NZ, Hasnain SE (2017) Mycobacterium tuberculosis peptidyl-prolyl isomerases are immunogenic, alter cytokine profile and aid in intracellular survival. Front Cell Infect Microbiol 7:1–9CrossRefGoogle Scholar
  40. Pang SS, Le YY (2006) Role of resistin in inflammation and inflammation-related diseases. Cell Mol Immunol 3:29–34PubMedGoogle Scholar
  41. Patel SD, Rajala MW, Rossetti L, Scherer PE, Shapiro L (2004) Disulfide-dependent multimeric assembly of resistin family hormones. Science 304:1154–1158CrossRefGoogle Scholar
  42. Peetermans WE, Raats CJI, Langermans JAM, Van Furth R (1994) Mycobacterial heat-shock protein 65 induces proinflammatory cytokines but does not activate human mononuclear phagocytes. Scand J Immunol 39:613–617CrossRefGoogle Scholar
  43. Perovic E, Mrdjen A, Harapin M, Tesija KA, Simundic AM (2017) Diagnostic and prognostic role of resistin and copeptin in acute ischemic stroke. Top Stroke Rehabil 24(8):614–618CrossRefGoogle Scholar
  44. Piatigorsky J (2007) Gene sharing and evolution: the diversity of protein functions. Harvard University Press, Cambridge, MA. isbn:9780674023413Google Scholar
  45. Reilly MP, Lehrke M, Wolfe ML, Rohatgi A, Lazar MA, Rader DJ (2005) Resistin is an inflammatory marker of atherosclerosis in humans. Circulation 111:932–939CrossRefGoogle Scholar
  46. Ritossa F (1962) A new puffing pattern induced by temperature shock and DNP in drosophila. Experientia 18:571–573CrossRefGoogle Scholar
  47. Saitoh T, Tun-Kyi A, Ryo A, Yamamoto M, Finn G, Fujita T, Akira S, Yamamoto N, Lu KP, Yamaoka S (2006) Negative regulation of interferon-regulatory factor 3–dependent innate antiviral response by the prolylisomerase Pin1. Nat Immunol 7:598–605CrossRefGoogle Scholar
  48. Schaffler A, Scholmerich J (2010) Innate immunity and adipose tissue biology. Trends Immunol 31:228–235CrossRefGoogle Scholar
  49. Schiene-Fischer C, Aumüller T, Fischer G (2013) Peptide bond cis/trans isomerases: a biocatalysis perspective of conformational dynamics in proteins. Top Curr Chem 328:35–67CrossRefGoogle Scholar
  50. Scholz C, Mücke M, Rape M, Pecht A, Pahl A, Bang H, Schmid FX (1998) Recognition of protein substrates by the prolylisomerase trigger factor is independent of proline residues. J Mol Biol 277:723–732CrossRefGoogle Scholar
  51. Sharma AD, Singh P (2003) Effect of water stress on expression of a 20 kD cyclophilin-like protein in drought susceptible and tolerant cultivars of sorghum. J Plant Biochem Biotechnol 12:77–80CrossRefGoogle Scholar
  52. Silswal N, Singh AK, Aruna B, Mukhopadhyay S, Ghosh S, Ehtesham NZ (2005) Human resistin stimulates the pro-inflammatory cytokines TNF-alpha and IL-12 in macrophages by NFκB-dependent pathway. Biochem Biophys Res Commun 334:1092–1101CrossRefGoogle Scholar
  53. Son YM, Ahn SM, Jang MS, Moon YS, Kim SH, Cho KK, Han SH, Yun CH (2008) Immunomodulatory effect of resistin in human dendritic cells stimulated with lipoteichoic acid from Staphylococcus aureus. Biochem Biophys Res Commun 376:599–604CrossRefGoogle Scholar
  54. Son YM, Ahn SM, Kim GR, Moon YS, Kim SH, Park Y-M, Lee WK, Min TS, Han SH, Yun C-H (2010) Resistin enhances the expansion of regulatory T cells through modulation of dendritic cells. BMC Immunol 11:33CrossRefGoogle Scholar
  55. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, Wright CM, Patel HR, Ahima RS, Lazar MA (2001a) The hormone resistin links obesity to diabetes. Nature 409:307–312CrossRefGoogle Scholar
  56. Steppan CM, Brown EJ, Wright CM, Bhat S, Banerjee RR, Dai CY, Enders GH, Silberg DG, Wen X, Wu GD, Lazar MA (2001b) A family of tissue-specific resistin-like molecules. Proc Natl Acad Sci U S A 98:502–506CrossRefGoogle Scholar
  57. Sun CA, Wu MH, Chu CH, Chou YC, Hsu GC, Yang T, Chou WY, Yu CP, Yu JC (2010) Adipocytokine resistin and breast cancer risk. Breast Cancer Res Treat 123:869–876CrossRefGoogle Scholar
  58. Suragani M, Aadinarayana VD, Pinjari AB, Tanneeru K, Guruprasad L, Banerjee S, Pandey S, Chaudhuri TK, Ehtesham NZ (2013) Human resistin, a proinflammatory cytokine, shows chaperone-like activity. Proc Natl Acad Sci U S A 110:20467–20472CrossRefGoogle Scholar
  59. Tan J, Huang Z, Guo X, Li T, Deng W (2014) Expression and significance of cyclophilin A in synovial fibroblasts from patients with rheumatoid arthritis. Zhonghua Yi Xue Za Zhi 94:1330–1333PubMedGoogle Scholar
  60. Trivedi DK, Ansari MW, Tuteja N (2013) Multiple abiotic stress responsive rice cyclophilin: (OsCYP-25) mediates a wide range of cellular responses. Commun Integr Biol 6:e25260CrossRefGoogle Scholar
  61. Unal CM, Steinert M (2014) Microbial peptidyl-prolylcis/trans isomerases (PPIases): virulence factors and potential alternative drug targets. Microbiol Mol Biol Rev 78:544–571CrossRefGoogle Scholar
  62. Wang J-H, Lee C-J, Yang C-F, Chen Y-C, Hsu B-G (2017) Serum resistin as an independent marker of aortic stiffness in patients with coronary artery disease. PLoS One 12:e0183123CrossRefGoogle Scholar
  63. Wu X, Wilcox CB, Devasahayam G, Hackett RL, Arévalo-Rodríguez M, Cardenas ME, Heitman J, Hanes SD (2000) The Ess1 prolylisomerase is linked to chromatin remodeling complexes and the general transcription machinery. EMBO J 19:3727–3738CrossRefGoogle Scholar
  64. Yaffe MB (1997) Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science 278:1957–1960CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Saurabh Pandey
    • 1
    • 2
  • Javeed Ahmad
    • 1
  • Nasreen Zafar Ehtesham
    • 1
  1. 1.Inflammation Biology and Cell Signaling LaboratoryNational Institute of PathologyNew DelhiIndia
  2. 2.Perelman School of MedicineUniversity of PennsylvaniaPhiladelphiaUSA

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