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Role of Heat Shock Factor 1 in HIV

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Heat Shock Proteins in Inflammatory Diseases

Part of the book series: Heat Shock Proteins ((HESP,volume 22))

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Abbreviations

AIDS:

acquired immune deficiency syndrome

AP-1:

activator protein 1

APOBEC3G:

apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3G

BRG1:

brahma related gene 1

CaMK II:

calcium/calmodulin-dependent protein kinase II

CBP:

CREB-binding protein

CHIP:

carboxy terminus of Hsp70-binding protein

CK2:

casein kinase 2

CREB:

cyclic AMP response element-binding protein

DBD:

deoxyribonucleic acid binding domain

ELL2:

eleven nineteen lysine-rich leukemia gene

ER stress:

endoplasmic reticulum stress

FACT:

facilitates chromatin transcription

GM-CSF:

granulocyte-macrophage colony-stimulating factor

HAART:

highly active antiretroviral therapy

HADCi:

histone deacetylase inhibitors

HIV:

human immunodeficiency virus

HO-1:

heme oxygenase-1

HR:

heptad repeats

HSE:

heat shock element

HSF1:

heat shock factor 1

HSFs:

heat shock factors

Hsp:

heat shock proteins

Hsp90:

heat shock protein 90

HSR:

heat shock response

IKKγ:

IκB phosphorylation kinase γ

LEDGF:

lens epithelial-derived growth factor

LEF-1:

lymphoid enhancer-binding factor 1

LPS:

lipopolysaccharide

LRAs:

latency reversing agents

LTR:

long terminal repeat

MAPK:

mitogen-activated protein kinase

MNSF-β:

monoclonal nonspecific suppressor factor β

mTOR:

mammalian target of rapamycin

NF-AT:

nuclear factor of activated T cells

NF-κB:

nuclear factor kappa-B

PARP1:

poly (ADP-ribose) polymerase 1

PIC:

preintegration complex

PIs:

proteasome inhibitors

PKA:

protein kinase A

PKC:

protein kinase C

PLK1:

polo-like kinase 1

PPARγ:

peroxisome proliferation activated receptor γ

PSMD:

26S proteasome non-ATPase regulatory subunit

p-TEFb:

positive transcription elongation factor b

REACT:

reiterative enrichment and authentication of CRISPRi targets

RPA:

replication protein A

SIRT1:

sirtuin1

SIV:

simian immunodeficiency virus

Sp1:

specificity protein 1

STAT5:

signal transducer and activator of transcription 5

TAD:

transcriptional activation domain

References

  1. Abdel-Hameed EA, Ji H, Shata MT (2016) HIV-induced epigenetic alterations in host cells. Adv Exp Med Biol 879:27–38

    Article  CAS  PubMed  Google Scholar 

  2. Agostini I, Popov S, Li J, Dubrovsky L, Hao T, Bukrinsky M (2000) Heat-shock protein 70 can replace viral protein R of HIV-1 during nuclear import of the viral preintegration complex. Exp Cell Res 259(2):398–403

    Article  CAS  PubMed  Google Scholar 

  3. Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 11(8):545–555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Al-Harti L, Joseph J, Nath A (2018) Astrocytes as an HIV CNS reservoir: highlights and reflections of an NIMH-sponsored symposium. J Neurovirol 24(6):665–669

    Article  PubMed  PubMed Central  Google Scholar 

  5. Ali A, Farooqui SR, Banerjea AC (2019) The host cell ubiquitin ligase protein CHIP is a potent suppressor of HIV-1 replication. J Biol Chem 294(18):7283–7295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Allen AG, Chung CH, Atkins A, Dampier W, Khalili K, Nonnemacher MR, Wigdahl B (2018) Gene editing of HIV-1 co-receptors to prevent and/or cure virus infection. Front Microbiol 9:2940

    Article  PubMed  PubMed Central  Google Scholar 

  7. Alvarez-Carbonell D, Garcia-Mesa Y, Milne S, Das B, Dobrowolski C, Rojas R, Karn J (2017) Toll-like receptor 3 activation selectively reverses HIV latency in microglial cells. Retrovirology 14(1):9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Alvarez-Carbonell D, Ye FC, Ramanath N, Dobrowolski C, Karn J (2019) The glucocorticoid receptor is a critical regulator of HIV latency in human microglial cells. J Neuroimmune Pharmacol 14(1):94–109

    Article  PubMed  Google Scholar 

  9. Anand D, Agrawal SA, Slavotinek A, Lachke SA (2018) Mutation update of transcription factor genes FOXE3, HSF4, MAF, and PITX3 causing cataracts and other developmental ocular defects. Hum Mutat 39(4):471–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Anckar J, Hietakangas V, Denessiouk K, Thiele DJ, Johnson MS, Sistonen L (2006) Inhibition of DNA binding by differential sumoylation of heat shock factors. Mol Cell Biol 26(3):955–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Anderson I, Low JS, Weston S, Weinberger M, Zhyvoloup A, Labokha AA, Corazza G, Kitson RA, Moody CJ, Marcello A, Fassati A (2014) Heat shock protein 90 controls HIV-1 reactivation from latency. Proc Natl Acad Sci U S A 111(15):E1528–E1537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Anraku I, Rajasuriar R, Dobbin C, Brown R, Lewin SR, Suhrbier A (2012) Circulating heat shock protein 60 levels are elevated in HIV patients and are reduced by anti-retroviral therapy. PLoS One 7(9):e45291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Aounallah M, Dagenais-Lussier X, El-Far M, Mehraj V, Jenabian MA, Routy JP, van Grevenynghe J (2016) Current topics in HIV pathogenesis, part 2: inflammation drives a Warburg-like effect on the metabolism of HIV-infected subjects. Cytokine Growth Factor Rev 28:1–10

    Article  CAS  PubMed  Google Scholar 

  14. Arrizabalaga J, Arazo P, Aguirrebengoa K, Garcia-Palomo D, Chocarro A, Labarga P, Munoz-Sanchez MJ, Echevarria S, Oteo JA, Uriz J, Letona S, Farinas MC, Peralta G, Pinilla J, Ferrer P, Alvarez ML, Iribarren JA (2007) Effectiveness and safety of simplification therapy with once-daily tenofovir, lamivudine, and efavirenz in HIV-1-infected patients with undetectable plasma viral load on HAART. HIV Clin Trials 8(5):328–336

    Article  PubMed  Google Scholar 

  15. Asamitsu K, Fujinaga K, Okamoto T (2018) HIV tat/P-TEFb interaction: a potential target for novel anti-HIV therapies. Molecules 23(4)

    Google Scholar 

  16. Avvakumov N, Nourani A, Cote J (2011) Histone chaperones: modulators of chromatin marks. Mol Cell 41(5):502–514

    Article  CAS  PubMed  Google Scholar 

  17. Ay E, Banati F, Mezei M, Bakos A, Niller HH, Buzas K, Minarovits J (2013) Epigenetics of HIV infection: promising research areas and implications for therapy. AIDS Rev 15(3):181–188

    PubMed  Google Scholar 

  18. Babaahmady K, Oehlmann W, Singh M, Lehner T (2007) Inhibition of human immunodeficiency virus type 1 infection of human CD4+ T cells by microbial HSP70 and the peptide epitope 407-426. J Virol 81(7):3354–3360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bacon CW, D’Orso I (2019) CDK9: a signaling hub for transcriptional control. Transcription 10(2):57–75

    Article  CAS  PubMed  Google Scholar 

  20. Bartholomeeusen K, Fujinaga K, Xiang Y, Peterlin BM (2013) Histone deacetylase inhibitors (HDACis) that release the positive transcription elongation factor b (P-TEFb) from its inhibitory complex also activate HIV transcription. J Biol Chem 288(20):14400–14407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bartz SR, Pauza CD, Ivanyi J, Jindal S, Welch WJ, Malkovsky M (1994) An Hsp60 related protein is associated with purified HIV and SIV. J Med Primatol 23(2–3):151–154

    Article  CAS  PubMed  Google Scholar 

  22. Bernhard W, Barreto K, Saunders A, Dahabieh MS, Johnson P, Sadowski I (2011) The Suv39H1 methyltransferase inhibitor chaetocin causes induction of integrated HIV-1 without producing a T cell response. FEBS Lett 585(22):3549–3554

    Article  CAS  PubMed  Google Scholar 

  23. Bharadwaj S, Ali A, Ovsenek N (1999) Multiple components of the HSP90 chaperone complex function in regulation of heat shock factor 1 in vivo. Mol Cell Biol 19(12):8033–8041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bieniasz PD, Grdina TA, Bogerd HP, Cullen BR (1998) Recruitment of a protein complex containing Tat and cyclin T1 to TAR governs the species specificity of HIV-1 Tat. EMBO J 17(23):7056–7065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Bolhassani A, Agi E (2019) Heat shock proteins in infection. Clin Chim Acta 498:90–100

    Article  CAS  PubMed  Google Scholar 

  26. Bonner JJ, Heyward S, Fackenthal DL (1992) Temperature-dependent regulation of a heterologous transcriptional activation domain fused to yeast heat shock transcription factor. Mol Cell Biol 12(3):1021–1030

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Bonner JJ, Chen D, Storey K, Tushan M, Lea K (2000) Structural analysis of yeast HSF by site-specific crosslinking. J Mol Biol 302(3):581–592

    Article  CAS  PubMed  Google Scholar 

  28. Bosque A, Planelles V (2009) Induction of HIV-1 latency and reactivation in primary memory CD4+ T cells. Blood 113(1):58–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Brunet Simioni M, De Thonel A, Hammann A, Joly AL, Bossis G, Fourmaux E, Bouchot A, Landry J, Piechaczyk M, Garrido C (2009) Heat shock protein 27 is involved in SUMO-2/3 modification of heat shock factor 1 and thereby modulates the transcription factor activity. Oncogene 28(37):3332–3344

    Article  CAS  PubMed  Google Scholar 

  30. Buffalo CZ, Iwamoto Y, Hurley JH, Ren X (2019) How HIV Nef proteins hijack membrane traffic to promote infection. J Virol

    Google Scholar 

  31. Bukrinsky M, Zhao Y (2004) Heat-shock proteins reverse the G2 arrest caused by HIV-1 viral protein R. DNA Cell Biol 23(4):223–225

    Article  CAS  PubMed  Google Scholar 

  32. Burdon RH, Slater A, McMahon M, Cato AC (1982) Hyperthermia and the heat-shock proteins of HeLa cells. Br J Cancer 45(6):953–963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Cao Z, Zhu Y, Liu L, Wu S, Liu B, Zhuang J, Tong Y, Chen X, Xie Y, Nie K, Lu C, Ma X, Yang J (2018) Novel mutations in HSF4 cause congenital cataracts in Chinese families. BMC Med Genet 19(1):150

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Carrillo J, Clotet B, Blanco J (2018) Antibodies and antibody derivatives: new partners in HIV eradication strategies. Front Immunol 9:2429

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Cary DC, Fujinaga K, Peterlin BM (2016) Molecular mechanisms of HIV latency. J Clin Invest 126(2):448–454

    Article  PubMed  PubMed Central  Google Scholar 

  36. Chaudhary P, Khan SZ, Rawat P, Augustine T, Raynes DA, Guerriero V, Mitra D (2016) HSP70 binding protein 1 (HspBP1) suppresses HIV-1 replication by inhibiting NF-kappaB mediated activation of viral gene expression. Nucleic Acids Res 44(4):1613–1629

    Article  PubMed  Google Scholar 

  37. Chen Y, Barlev NA, Westergaard O, Jakobsen BK (1993) Identification of the C-terminal activator domain in yeast heat shock factor: independent control of transient and sustained transcriptional activity. EMBO J 12(13):5007–5018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Cheng X, Belshan M, Ratner L (2008) Hsp40 facilitates nuclear import of the human immunodeficiency virus type 2 Vpx-mediated preintegration complex. J Virol 82(3):1229–1237

    Article  CAS  PubMed  Google Scholar 

  39. Chou SD, Prince T, Gong J, Calderwood SK (2012) mTOR is essential for the proteotoxic stress response, HSF1 activation and heat shock protein synthesis. PLoS One 7(6):e39679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Chun TW, Stuyver L, Mizell SB, Ehler LA, Mican JA, Baseler M, Lloyd AL, Nowak MA, Fauci AS (1997) Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc Natl Acad Sci U S A 94(24):13193–13197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Chun TW, Engel D, Berrey MM, Shea T, Corey L, Fauci AS (1998) Early establishment of a pool of latently infected, resting CD4(+) T cells during primary HIV-1 infection. Proc Natl Acad Sci U S A 95(15):8869–8873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Contreras X, Barboric M, Lenasi T, Peterlin BM (2007) HMBA releases P-TEFb from HEXIM1 and 7SK snRNA via PI3K/Akt and activates HIV transcription. PLoS Pathog 3(10):1459–1469

    Article  CAS  PubMed  Google Scholar 

  43. Cribbs SK, Crothers K, Morris A (2019) Pathogenesis of HIV-related lung disease: immunity, infection, and inflammation. Physiol Rev

    Google Scholar 

  44. Cui X, Han J, Li J, Cui WW, Wu DD, Liu S, Xue W, Wang XX, Ma Y, Zhang J, Zhang J, Mu H, Zhang F, Hu Y (2018) Downregulation of heat shock factor 4 transcription activity via MAPKinase phosphorylation at serine 299. Int J Biochem Cell Biol 105:61–69

    Article  CAS  PubMed  Google Scholar 

  45. Cunningham AL, Dwyer DE, Mills J, Montagnier L (1996) Managing HIV. Part 3: mechanisms of disease. 3.1 structure and function of HIV. Med J Aust 164(3):161–165

    Article  CAS  PubMed  Google Scholar 

  46. Dai S, Tang Z, Cao J, Zhou W, Li H, Sampson S, Dai C (2015) Suppression of the HSF1-mediated proteotoxic stress response by the metabolic stress sensor AMPK. EMBO J 34(3):275–293

    Article  CAS  PubMed  Google Scholar 

  47. Daul CB, deShazo RD (1983) Acquired immune deficiency syndrome: an update and interpretation. Ann Allergy 51(3):351–361

    CAS  PubMed  Google Scholar 

  48. Dayalan Naidu S, Dinkova-Kostova AT (2017) Regulation of the mammalian heat shock factor 1. FEBS J 284(11):1606–1627

    Article  CAS  PubMed  Google Scholar 

  49. Dayalan Naidu S, Sutherland C, Zhang Y, Risco A, de la Vega L, Caunt CJ, Hastie CJ, Lamont DJ, Torrente L, Chowdhry S, Benjamin IJ, Keyse SM, Cuenda A, Dinkova-Kostova AT (2016) Heat shock factor 1 is a substrate for p38 mitogen-activated protein kinases. Mol Cell Biol 36(18):2403–2417

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. de Marco A, Carattoli A, Rozera C, Fortini D, Giorgi C, Belardo G, Amici C, Santoro MG (1998) Induction of the heat-shock response by antiviral prostaglandins in human cells infected with human immunodeficiency virus type 1. Eur J Biochem 256(2):334–341

    Article  CAS  PubMed  Google Scholar 

  51. Deeks SG (2012) HIV: shock and kill. Nature 487(7408):439–440

    Article  CAS  PubMed  Google Scholar 

  52. Donahue DA, Wainberg MA (2013) Cellular and molecular mechanisms involved in the establishment of HIV-1 latency. Retrovirology 10:11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Drees BL, Grotkopp EK, Nelson HC (1997) The GCN4 leucine zipper can functionally substitute for the heat shock transcription factor’s trimerization domain. J Mol Biol 273(1):61–74

    Article  CAS  PubMed  Google Scholar 

  54. Dubrez L, Causse S, Borges Bonan N, Dumetier B, Garrido C (2019) Heat-shock proteins: chaperoning DNA repair. Oncogene

    Google Scholar 

  55. Dukay B, Csoboz B, Toth ME (2019) Heat-shock proteins in neuroinflammation. Front Pharmacol 10:920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Eilebrecht S, Benecke BJ, Benecke AG (2017) Latent HIV-1 TAR regulates 7SK-responsive P-TEFb target genes and targets cellular immune responses in the absence of tat. Genomics Proteomics Bioinformatics 15(5):313–323

    Article  PubMed  PubMed Central  Google Scholar 

  57. Elsing AN, Aspelin C, Bjork JK, Bergman HA, Himanen SV, Kallio MJ, Roos-Mattjus P, Sistonen L (2014) Expression of HSF2 decreases in mitosis to enable stress-inducible transcription and cell survival. J Cell Biol 206(6):735–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Espigares E, Bueno A, Hernandez J, Garcia F, Luna JD, Espigares M, Galvez R (2006) Levels of HSP70 in HIV(+) patients in different viroimmunological states. J Med Virol 78(3):318–323

    Article  CAS  PubMed  Google Scholar 

  59. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  CAS  PubMed  Google Scholar 

  60. Feng H, Wang S, Guo L, Punekar AS, Ladenstein R, Wang DC, Liu W (2016) MD simulation of high-resolution X-ray structures reveals post-translational modification dependent conformational changes in HSF-DNA interaction. Protein Cell 7(12):916–920

    Article  PubMed  PubMed Central  Google Scholar 

  61. Fernandez G, Zeichner SL (2010) Cell line-dependent variability in HIV activation employing DNMT inhibitors. Virol J 7:266

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Filone CM, Caballero IS, Dower K, Mendillo ML, Cowley GS, Santagata S, Rozelle DK, Yen J, Rubins KH, Hacohen N, Root DE, Hensley LE, Connor J (2014) The master regulator of the cellular stress response (HSF1) is critical for orthopoxvirus infection. PLoS Pathog 10(2):e1003904

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Finlayson-Trick E, Connors J, Stadnyk A, Limbergen JV (2018) Regulation of antimicrobial pathways by endogenous heat shock proteins in gastrointestinal disorders. Gastrointest Dis 1(1):39–56

    Article  Google Scholar 

  64. Finzi D, Hermankova M, Pierson T, Carruth LM, Buck C, Chaisson RE, Quinn TC, Chadwick K, Margolick J, Brookmeyer R, Gallant J, Markowitz M, Ho DD, Richman DD, Siliciano RF (1997) Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278(5341):1295–1300

    Article  CAS  PubMed  Google Scholar 

  65. Fritah S, Col E, Boyault C, Govin J, Sadoul K, Chiocca S, Christians E, Khochbin S, Jolly C, Vourc’h C (2009) Heat-shock factor 1 controls genome-wide acetylation in heat-shocked cells. Mol Biol Cell 20(23):4976–4984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Fujimoto M, Nakai A (2010) The heat shock factor family and adaptation to proteotoxic stress. FEBS J 277(20):4112–4125

    Article  CAS  PubMed  Google Scholar 

  67. Fujimoto M, Takaki E, Takii R, Tan K, Prakasam R, Hayashida N, Iemura S, Natsume T, Nakai A (2012) RPA assists HSF1 access to nucleosomal DNA by recruiting histone chaperone FACT. Mol Cell 48(2):182–194

    Article  CAS  PubMed  Google Scholar 

  68. Fujinaga K, Taube R, Wimmer J, Cujec TP, Peterlin BM (1999) Interactions between human cyclin T, Tat, and the transactivation response element (TAR) are disrupted by a cysteine to tyrosine substitution found in mouse cyclin T. Proc Natl Acad Sci U S A 96(4):1285–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Gao XC, Zhou CJ, Zhou ZR, Wu M, Cao CY, Hu HY (2012) The C-terminal helices of heat shock protein 70 are essential for J-domain binding and ATPase activation. J Biol Chem 287(8):6044–6052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Gelmedin V, Delaney A, Jennelle L, Hawdon JM (2015) Expression profile of heat shock response factors during hookworm larval activation and parasitic development. Mol Biochem Parasitol 202(1):1–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Goodson ML, Hong Y, Rogers R, Matunis MJ, Park-Sarge OK, Sarge KD (2001) Sumo-1 modification regulates the DNA binding activity of heat shock transcription factor 2, a promyelocytic leukemia nuclear body associated transcription factor. J Biol Chem 276(21):18513–18518

    Article  CAS  PubMed  Google Scholar 

  72. Green M, Schuetz TJ, Sullivan EK, Kingston RE (1995) A heat shock-responsive domain of human HSF1 that regulates transcription activation domain function. Mol Cell Biol 15(6):3354–3362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Guettouche T, Boellmann F, Lane WS, Voellmy R (2005) Analysis of phosphorylation of human heat shock factor 1 in cells experiencing a stress. BMC Biochem 6:4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Gurer C, Cimarelli A, Luban J (2002) Specific incorporation of heat shock protein 70 family members into primate lentiviral virions. J Virol 76(9):4666–4670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Hakre S, Chavez L, Shirakawa K, Verdin E (2011) Epigenetic regulation of HIV latency. Curr Opin HIV AIDS 6(1):19–24

    Article  PubMed  Google Scholar 

  76. Harrison CJ, Bohm AA, Nelson HC (1994) Crystal structure of the DNA binding domain of the heat shock transcription factor. Science 263(5144):224–227

    Article  CAS  PubMed  Google Scholar 

  77. Hashimoto K, Baba M, Gohnai K, Sato M, Shigeta S (1996) Heat shock induces HIV-1 replication in chronically infected promyelocyte cell line OM10.1. Arch Virol 141(3–4):439–447

    Article  CAS  PubMed  Google Scholar 

  78. Hietakangas V, Ahlskog JK, Jakobsson AM, Hellesuo M, Sahlberg NM, Holmberg CI, Mikhailov A, Palvimo JJ, Pirkkala L, Sistonen L (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock factor 1. Mol Cell Biol 23(8):2953–2968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Hileman CO, Funderburg NT (2017) Inflammation, immune activation, and antiretroviral therapy in HIV. Curr HIV/AIDS Rep 14(3):93–100

    Article  PubMed  PubMed Central  Google Scholar 

  80. Hilgarth RS, Sarge KD (2005) Detection of sumoylated proteins. Methods Mol Biol 301:329–338

    CAS  PubMed  Google Scholar 

  81. Hilgarth RS, Murphy LA, O’Connor CM, Clark JA, Park-Sarge OK, Sarge KD (2004) Identification of Xenopus heat shock transcription factor-2: conserved role of sumoylation in regulating deoxyribonucleic acid-binding activity of heat shock transcription factor-2 proteins. Cell Stress Chaperones 9(2):214–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Hong Y, Rogers R, Matunis MJ, Mayhew CN, Goodson ML, Park-Sarge OK, Sarge KD (2001) Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification. J Biol Chem 276(43):40263–40267

    Article  CAS  PubMed  Google Scholar 

  83. Hotter D, Bosso M, Jonsson KL, Krapp C, Sturzel CM, Das A, Littwitz-Salomon E, Berkhout B, Russ A, Wittmann S, Gramberg T, Zheng Y, Martins LJ, Planelles V, Jakobsen MR, Hahn BH, Dittmer U, Sauter D, Kirchhoff F (2019) IFI16 targets the transcription factor Sp1 to suppress HIV-1 transcription and latency reactivation. Cell Host Microbe 25(6):858–872 e813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Hu YZ, Zhang J, Li S, Wang C, Chu L, Zhang Z, Ma Z, Wang M, Jiang Q, Liu G, Qi Y, Ma Y (2013) The transcription activity of heat shock factor 4b is regulated by FGF2. Int J Biochem Cell Biol 45(2):317–325

    Article  CAS  PubMed  Google Scholar 

  85. Huang CB, Alimova YV, Strange S, Ebersole JL (2011) Polybacterial challenge enhances HIV reactivation in latently infected macrophages and dendritic cells. Immunology 132(3):401–409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Huang CY, Kuo CH, Pai PY, Ho TJ, Lin YM, Chen RJ, Tsai FJ, Vijaya Padma V, Kuo WW, Huang CY (2018) Inhibition of HSF2 SUMOylation via MEL18 upregulates IGF-IIR and leads to hypertension-induced cardiac hypertrophy. Int J Cardiol 257:283–290

    Article  PubMed  Google Scholar 

  87. Ikeda T, Molan AM, Jarvis MC, Carpenter MA, Salamango DJ, Brown WL, Harris RS (2019) HIV-1 restriction by endogenous APOBEC3G in the myeloid cell line THP-1. J Gen Virol 100(7):1140–1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Iordanskiy S, Zhao Y, Dubrovsky L, Iordanskaya T, Chen M, Liang D, Bukrinsky M (2004a) Heat shock protein 70 protects cells from cell cycle arrest and apoptosis induced by human immunodeficiency virus type 1 viral protein R. J Virol 78(18):9697–9704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Iordanskiy S, Zhao Y, DiMarzio P, Agostini I, Dubrovsky L, Bukrinsky M (2004b) Heat-shock protein 70 exerts opposing effects on Vpr-dependent and Vpr-independent HIV-1 replication in macrophages. Blood 104(6):1867–1872

    Article  CAS  PubMed  Google Scholar 

  90. Izumi M (2019) Heat shock proteins support refolding and shredding of misfolded proteins. Plant Physiol 180(4):1777–1778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Jacob P, Hirt H, Bendahmane A (2017) The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnol J 15(4):405–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Jaeger AM, Pemble CW t, Sistonen L, Thiele DJ (2016) Structures of HSF2 reveal mechanisms for differential regulation of human heat-shock factors. Nat Struct Mol Biol 23(2):147–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Jiang G, Dandekar S (2015) Targeting NF-kappaB signaling with protein kinase C agonists as an emerging strategy for combating HIV latency. AIDS Res Hum Retrovir 31(1):4–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Jiang S, Wu B, Jiang L, Zhang M, Lu Y, Wang S, Yan F, Xin X (2019) Triticum aestivum heat shock protein 23.6 interacts with the coat protein of wheat yellow mosaic virus. Virus Genes 55(2):209–217

    Article  CAS  PubMed  Google Scholar 

  95. Joshi P, Stoddart CA (2011) Impaired infectivity of ritonavir-resistant HIV is rescued by heat shock protein 90AB1. J Biol Chem 286(28):24581–24592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Joshi P, Sloan B, Torbett BE, Stoddart CA (2013) Heat shock protein 90AB1 and hyperthermia rescue infectivity of HIV with defective cores. Virology 436(1):162–172

    Article  CAS  PubMed  Google Scholar 

  97. Joshi P, Maidji E, Stoddart CA (2016) Inhibition of heat shock protein 90 prevents HIV rebound. J Biol Chem 291(19):10332–10346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Kalderon B, Kogan G, Bubis E, Pines O (2015) Cytosolic Hsp60 can modulate proteasome activity in yeast. J Biol Chem 290(6):3542–3551

    Article  CAS  PubMed  Google Scholar 

  99. Kessing CF, Nixon CC, Li C, Tsai P, Takata H, Mousseau G, Ho PT, Honeycutt JB, Fallahi M, Trautmann L, Garcia JV, Valente ST (2017) In vivo suppression of HIV rebound by didehydro-cortistatin A, a “block-and-lock” strategy for HIV-1 treatment. Cell Rep 21(3):600–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Kestler HW 3rd, Ringler DJ, Mori K, Panicali DL, Sehgal PK, Daniel MD, Desrosiers RC (1991) Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65(4):651–662

    Article  CAS  PubMed  Google Scholar 

  101. Khachatoorian R, Cohn W, Buzzanco A, Riahi R, Arumugaswami V, Dasgupta A, Whitelegge JP, French SW (2018) HSP70 Copurifies with Zika virus particles. Virology 522:228–233

    Article  CAS  PubMed  Google Scholar 

  102. Khoury G, Mota TM, Li S, Tumpach C, Lee MY, Jacobson J, Harty L, Anderson JL, Lewin SR, Purcell DFJ (2018a) HIV latency reversing agents act through tat post translational modifications. Retrovirology 15(1):36

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Khoury G, Darcis G, Lee MY, Bouchat S, Van Driessche B, Purcell DFJ, Van Lint C (2018b) The molecular biology of HIV latency. Adv Exp Med Biol 1075:187–212

    Article  CAS  PubMed  Google Scholar 

  104. Kim SA, Yoon JH, Lee SH, Ahn SG (2005) Polo-like kinase 1 phosphorylates heat shock transcription factor 1 and mediates its nuclear translocation during heat stress. J Biol Chem 280(13):12653–12657

    Article  CAS  PubMed  Google Scholar 

  105. Klaus BD, Grodesky MJ (1997) HIV and HAART in 1997. Highly active antiretroviral therapy. Nurse Pract 22(8):139–142

    Article  CAS  PubMed  Google Scholar 

  106. Kong FC, Ma CL, Zhong MK (2019) Epigenetic effects mediated by antiepileptic drugs and their potential application. Curr Neuropharmacol

    Google Scholar 

  107. Kourtis N, Moubarak RS, Aranda-Orgilles B, Lui K, Aydin IT, Trimarchi T, Darvishian F, Salvaggio C, Zhong J, Bhatt K, Chen EI, Celebi JT, Lazaris C, Tsirigos A, Osman I, Hernando E, Aifantis I (2015) FBXW7 modulates cellular stress response and metastatic potential through HSF1 post-translational modification. Nat Cell Biol 17(3):322–332

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  108. Kuhnel A, Schilling D, Combs SE, Haller B, Schwab M, Multhoff G (2019) Radiosensitization of HSF-1 knockdown lung cancer cells by low concentrations of Hsp90 Inhibitor NVP-AUY922. Cells 8(10)

    Google Scholar 

  109. Kumar M, Mitra D (2005) Heat shock protein 40 is necessary for human immunodeficiency virus-1 Nef-mediated enhancement of viral gene expression and replication. J Biol Chem 280(48):40041–40050

    Article  CAS  PubMed  Google Scholar 

  110. Kumar M, Rawat P, Khan SZ, Dhamija N, Chaudhary P, Ravi DS, Mitra D (2011) Reciprocal regulation of human immunodeficiency virus-1 gene expression and replication by heat shock proteins 40 and 70. J Mol Biol 410(5):944–958

    Article  CAS  PubMed  Google Scholar 

  111. Lahaye X, Vidy A, Fouquet B, Blondel D (2012) Hsp70 protein positively regulates rabies virus infection. J Virol 86(9):4743–4751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Lampi Y, Van Looveren D, Vranckx LS, Thiry I, Bornschein S, Debyser Z, Gijsbers R (2019) Targeted editing of the PSIP1 gene encoding LEDGF/p75 protects cells against HIV infection. Sci Rep 9(1):2389

    Article  PubMed  PubMed Central  Google Scholar 

  113. Lang BJ, Guerrero-Gimenez ME, Prince TL, Ackerman A, Bonorino C, Calderwood SK (2019) Heat shock proteins are essential components in transformation and tumor progression: cancer cell intrinsic pathways and beyond. Int J Mol Sci 20(18)

    Google Scholar 

  114. Larson JS, Schuetz TJ, Kingston RE (1995) In vitro activation of purified human heat shock factor by heat. Biochemistry 34(6):1902–1911

    Article  CAS  PubMed  Google Scholar 

  115. Li GC (1983) Induction of thermotolerance and enhanced heat shock protein synthesis in Chinese hamster fibroblasts by sodium arsenite and by ethanol. (0021-9541 (Print)): 115(112):116–122

    Google Scholar 

  116. Li Z, Guo J, Wu Y, Zhou Q (2013) The BET bromodomain inhibitor JQ1 activates HIV latency through antagonizing Brd4 inhibition of Tat-transactivation. Nucleic Acids Res 41(1):277–287

    Article  CAS  PubMed  Google Scholar 

  117. Li Z, Wu J, Chavez L, Hoh R, Deeks SG, Pillai SK, Zhou Q (2019) Reiterative enrichment and authentication of CRISPRi targets (REACT) identifies the proteasome as a key contributor to HIV-1 latency. PLoS Pathog 15(1):e1007498

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  118. Liang T, Zhang X, Lai F, Lin J, Zhou C, Xu X, Tan X, Liu S, Li L (2019) A novel bromodomain inhibitor, CPI-203, serves as an HIV-1 latency-reversing agent by activating positive transcription elongation factor b. Biochem Pharmacol 164:237–251

    Article  CAS  PubMed  Google Scholar 

  119. Liebelt F, Sebastian RM, Moore CL, Mulder MPC, Ovaa H, Shoulders MD, Vertegaal ACO (2019) SUMOylation and the HSF1-regulated chaperone network converge to promote proteostasis in response to heat shock. Cell Rep 26(1):236–249 e234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Lin J, Zhang X, Lu W, Xu X, Pan X, Liang T, Duan S, Chen Y, Li L, Liu S (2018) PR-957, a selective immunoproteasome inhibitor, reactivates latent HIV-1 through p-TEFb activation mediated by HSF-1. Biochem Pharmacol 156:511–523

    Article  CAS  PubMed  Google Scholar 

  121. Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191

    Article  CAS  PubMed  Google Scholar 

  122. Littlefield O, Nelson HC (1999) A new use for the ‘wing’ of the ‘winged’ helix-turn-helix motif in the HSF-DNA cocrystal. Nat Struct Biol 6(5):464–470

    Article  CAS  PubMed  Google Scholar 

  123. Liu R, Lin Y, Jia R, Geng Y, Liang C, Tan J, Qiao W (2014) HIV-1 Vpr stimulates NF-kappaB and AP-1 signaling by activating TAK1. Retrovirology 11:45

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Liu Q, Liang C, Zhou L (2019) Structural and functional analysis of the Hsp70/Hsp40 chaperone system. Protein Sci

    Google Scholar 

  125. Loison F, Debure L, Nizard P, le Goff P, Michel D, le Drean Y (2006) Up-regulation of the clusterin gene after proteotoxic stress: implication of HSF1-HSF2 heterocomplexes. Biochem J 395(1):223–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Lopez AP, Kugelman JR, Garcia-Rivera J, Urias E, Salinas SA, Fernandez-Zapico ME, Llano M (2016) The structure-specific recognition protein 1 associates with lens epithelium-derived growth factor proteins and modulates HIV-1 replication. J Mol Biol 428(14):2814–2831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Low JS, Fassati A (2014) Hsp90: a chaperone for HIV-1. Parasitology 141(9):1192–1202

    Article  CAS  PubMed  Google Scholar 

  128. Madlala P, Gijsbers R, Christ F, Hombrouck A, Werner L, Mlisana K, An P, Abdool Karim SS, Winkler CA, Debyser Z, Ndung’u T (2011) Association of polymorphisms in the LEDGF/p75 gene (PSIP1) with susceptibility to HIV-1 infection and disease progression. AIDS 25(14):1711–1719

    Article  CAS  PubMed  Google Scholar 

  129. Madrid-Elena N, Garcia-Bermejo ML, Serrano-Villar S, Diaz-de Santiago A, Sastre B, Gutierrez C, Dronda F, Coronel Diaz M, Dominguez E, Lopez-Huertas MR, Hernandez-Novoa B, Moreno S (2018) Maraviroc is associated with latent HIV-1 reactivation through NF-kappaB activation in resting CD4(+) T cells from HIV-infected individuals on suppressive antiretroviral therapy. J Virol 92(9)

    Google Scholar 

  130. Mammano F, Petit C, Clavel F (1998) Resistance-associated loss of viral fitness in human immunodeficiency virus type 1: phenotypic analysis of protease and gag coevolution in protease inhibitor-treated patients. J Virol 72(9):7632–7637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Martine P, Rebe C (2019) Heat shock proteins and inflammasomes. Int J Mol Sci 20(18)

    Google Scholar 

  132. Martinez-Bonet M, Clemente MI, Alvarez S, Diaz L, Garcia-Alonso D, Munoz E, Moreno S, Munoz-Fernandez MA (2015) Antiretroviral drugs do not interfere with bryostatin-mediated HIV-1 latency reversal. Antivir Res 123:163–171

    Article  CAS  PubMed  Google Scholar 

  133. Mbonye U, Karn J (2014) Transcriptional control of HIV latency: cellular signaling pathways, epigenetics, happenstance and the hope for a cure. Virology 454–455:328–339

    Article  PubMed  CAS  Google Scholar 

  134. Merkling SH, Overheul GJ, van Mierlo JT, Arends D, Gilissen C, van Rij RP (2015) The heat shock response restricts virus infection in Drosophila. Sci Rep 5:12758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12(24):3788–3796

    Article  CAS  PubMed  Google Scholar 

  136. Morimoto RI, Kline MP, Bimston DN, Cotto JJ (1997) The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem 32:17–29

    CAS  PubMed  Google Scholar 

  137. Multhoff G (2006) Heat shock proteins in immunity. Handb Exp Pharmacol (172):279–304

    Google Scholar 

  138. Murshid A, Chou SD, Prince T, Zhang Y, Bharti A, Calderwood SK (2010) Protein kinase a binds and activates heat shock factor 1. PLoS One 5(11):e13830

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  139. Murshid A, Prince TL, Lang B, Calderwood SK (2018) Role of heat shock factors in stress-induced transcription. Methods Mol Biol 1709:23–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Nakai A, Morimoto RI (1993) Characterization of a novel chicken heat shock transcription factor, heat shock factor 3, suggests a new regulatory pathway. Mol Cell Biol 13(4):1983–1997

    CAS  PubMed  PubMed Central  Google Scholar 

  141. Nakai A, Tanabe M, Kawazoe Y, Inazawa J, Morimoto RI, Nagata K (1997) HSF4, a new member of the human heat shock factor family which lacks properties of a transcriptional activator. Mol Cell Biol 17(1):469–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Nakamura M, Notsu K, Nakagawa M (2019) Heat shock protein 60 negatively regulates the biological functions of ubiquitin-like protein MNSFbeta in macrophages. Mol Cell Biochem 456(1-2):29–39

    Article  CAS  PubMed  Google Scholar 

  143. O’Keeffe B, Fong Y, Chen D, Zhou S, Zhou Q (2000) Requirement for a kinase-specific chaperone pathway in the production of a Cdk9/cyclin T1 heterodimer responsible for P-TEFb-mediated tat stimulation of HIV-1 transcription. J Biol Chem 275(1):279–287

    Article  PubMed  Google Scholar 

  144. Ortner V, Ludwig A, Riegel E, Dunzinger S, Czerny T (2015) An artificial HSE promoter for efficient and selective detection of heat shock pathway activity. Cell Stress Chaperones 20(2):277–288

    Article  CAS  PubMed  Google Scholar 

  145. Ostling P, Bjork JK, Roos-Mattjus P, Mezger V, Sistonen L (2007) Heat shock factor 2 (HSF2) contributes to inducible expression of hsp genes through interplay with HSF1. J Biol Chem 282(10):7077–7086

    Article  PubMed  CAS  Google Scholar 

  146. Pan XY, Zhao W, Zeng XY, Lin J, Li MM, Shen XT, Liu SW (2016a) Heat shock factor 1 mediates latent HIV reactivation. Sci Rep 6:26294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Pan XY, Zhao W, Wang CY, Lin J, Zeng XY, Ren RX, Wang K, Xun TR, Shai Y, Liu SW (2016b) Heat shock protein 90 facilitates latent HIV reactivation through maintaining the function of positive transcriptional elongation factor b (p-TEFb) under proteasome inhibition. J Biol Chem 291(50):26177–26187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Pan X, Lin J, Zeng X, Li W, Wu W, Lu WZ, Liu J, Liu S (2018) Heat shock factor 1 suppresses the HIV-induced inflammatory response by inhibiting nuclear factor-kappaB. Cell Immunol 327:26–35

    Article  CAS  PubMed  Google Scholar 

  149. Pan T, Song Z, Wu L, Liu G, Ma X, Peng Z, Zhou M, Liang L, Liu B, Liu J, Zhang J, Zhang X, Huang R, Zhao J, Li Y, Ling X, Luo Y, Tang X, Cai W, Deng K, Li L, Zhang H (2019) USP49 potently stabilizes APOBEC3G protein by removing ubiquitin and inhibits HIV-1 replication. elife 8

    Google Scholar 

  150. Panfil AR, London JA, Green PL, Yoder KE (2018) CRISPR/Cas9 genome editing to disable the latent HIV-1 provirus. Front Microbiol 9:3107

    Article  PubMed  PubMed Central  Google Scholar 

  151. Parissi V, Calmels C, De Soultrait VR, Caumont A, Fournier M, Chaignepain S, Litvak S (2001) Functional interactions of human immunodeficiency virus type 1 integrase with human and yeast HSP60. J Virol 75(23):11344–11353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Peng W, Zhang Y, Zheng M, Cheng H, Zhu W, Cao CM, Xiao RP (2010) Cardioprotection by CaMKII-deltaB is mediated by phosphorylation of heat shock factor 1 and subsequent expression of inducible heat shock protein 70. Circ Res 106(1):102–110

    Article  CAS  PubMed  Google Scholar 

  153. Peng J, Li Y, Wang X, Deng S, Holland J, Yates E, Chen J, Gu H, Essandoh K, Mu X, Wang B, McNamara RK, Peng T, Jegga AG, Liu T, Nakamura T, Huang K, Perez-Tilve D, Fan GC (2018) An Hsp20-FBXO4 axis regulates adipocyte function through modulating PPARgamma ubiquitination. Cell Rep 23(12):3607–3620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Peppenelli MA, Miller MJ, Altman AM, Cojohari O, Chan GC (2018) Aberrant regulation of the Akt signaling network by human cytomegalovirus allows for targeting of infected monocytes. Antivir Res 158:13–24

    Article  CAS  PubMed  Google Scholar 

  155. Pierson T, McArthur J, Siliciano RF (2000) Reservoirs for HIV-1: mechanisms for viral persistence in the presence of antiviral immune responses and antiretroviral therapy. Annu Rev Immunol 18:665–708

    Article  CAS  PubMed  Google Scholar 

  156. Poccia F, Piselli P, Vendetti S, Bach S, Amendola A, Placido R, Colizzi V (1996) Heat-shock protein expression on the membrane of T cells undergoing apoptosis. Immunology 88(1):6–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Prohaszka Z, Daha MR, Susal C, Daniel V, Szlavik J, Banhegyi D, Nagy K, Varkonyi V, Horvath A, Ujhelyi E, Toth FD, Uray K, Hudecz F, Fust G (1999) C1q autoantibodies in HIV infection: correlation to elevated levels of autoantibodies against 60-kDa heat-shock proteins. Clin Immunol 90(2):247–255

    Article  CAS  PubMed  Google Scholar 

  158. Quagliarello V (1982) The acquired immunodeficiency syndrome: current status. Yale J Biol Med 55(5-6):443–452

    CAS  PubMed  PubMed Central  Google Scholar 

  159. Rabindran SK, Giorgi G, Clos J, Wu C (1991) Molecular cloning and expression of a human heat shock factor, HSF1. Proc Natl Acad Sci U S A 88(16):6906–6910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Rabindran SK, Haroun RI, Clos J, Wisniewski J, Wu C (1993) Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science 259(5092):230–234

    Article  CAS  PubMed  Google Scholar 

  161. Rasmussen TA, Tolstrup M, Moller HJ, Brinkmann CR, Olesen R, Erikstrup C, Laursen AL, Ostergaard L, Sogaard OS (2015) Activation of latent human immunodeficiency virus by the histone deacetylase inhibitor panobinostat: a pilot study to assess effects on the central nervous system. Open Forum Infect Dis 2(1):ofv037

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  162. Rawat P, Mitra D (2011) Cellular heat shock factor 1 positively regulates human immunodeficiency virus-1 gene expression and replication by two distinct pathways. Nucleic Acids Res 39(14):5879–5892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Raychaudhuri S, Loew C, Korner R, Pinkert S, Theis M, Hayer-Hartl M, Buchholz F, Hartl FU (2014) Interplay of acetyltransferase EP300 and the proteasome system in regulating heat shock transcription factor 1. Cell 156(5):975–985

    Article  CAS  PubMed  Google Scholar 

  164. Ritossa FM, Vonborstel RC (1964) Chromosome puffs in Drosophila induced by Ribonuclease. Science 145(3631):513–514

    Article  CAS  PubMed  Google Scholar 

  165. Roesch F, Meziane O, Kula A, Nisole S, Porrot F, Anderson I, Mammano F, Fassati A, Marcello A, Benkirane M, Schwartz O (2012) Hyperthermia stimulates HIV-1 replication. PLoS Pathog 8(7):e1002792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Saju JM, Hossain MS, Liew WC, Pradhan A, Thevasagayam NM, Tan LSE, Anand A, Olsson PE, Orban L (2018) Heat shock factor 5 is essential for spermatogenesis in Zebrafish. Cell Rep 25(12):3252–3261. e3254

    Article  CAS  PubMed  Google Scholar 

  167. Sakamoto N, Kokura S, Okuda T, Hattori T, Katada K, Isozaki Y, Nakabe N, Handa O, Takagi T, Ishikawa T, Naito Y, Yoshida N, Yoshikawa T (2005) Heme oxygenase-1 (Hsp32) is involved in the protection of small intestine by whole body mild hyperthermia from ischemia/reperfusion injury in rat. Int J Hyperth 21(7):603–614

    Article  CAS  Google Scholar 

  168. Sakurai H, Takemori Y (2007) Interaction between heat shock transcription factors (HSFs) and divergent binding sequences: binding specificities of yeast HSFs and human HSF1. J Biol Chem 282(18):13334–13341

    Article  CAS  PubMed  Google Scholar 

  169. Salerno L, Floresta G, Ciaffaglione V, Gentile D, Margani F, Turnaturi R, Rescifina A, Pittala V (2019) Progress in the development of selective heme oxygenase-1 inhibitors and their potential therapeutic application. Eur J Med Chem 167:439–453

    Article  CAS  PubMed  Google Scholar 

  170. Sandqvist A, Bjork JK, Akerfelt M, Chitikova Z, Grichine A, Vourc’h C, Jolly C, Salminen TA, Nymalm Y, Sistonen L (2009) Heterotrimerization of heat-shock factors 1 and 2 provides a transcriptional switch in response to distinct stimuli. Mol Biol Cell 20(5):1340–1347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Saotome M, Horikoshi N, Urano K, Kujirai T, Yuzurihara H, Kurumizaka H, Kagawa W (2019) Structure determination of the nucleosome core particle by selenium SAD phasing. Acta Crystallogr D Struct Biol 75(Pt 10):930–936

    Article  CAS  PubMed  Google Scholar 

  172. Sattentau QJ, Dalgleish AG, Weiss RA, Beverley PC (1986) Epitopes of the CD4 antigen and HIV infection. Science 234(4780):1120–1123

    Article  CAS  PubMed  Google Scholar 

  173. Schrager LK, D’Souza MP (1998) Cellular and anatomical reservoirs of HIV-1 in patients receiving potent antiretroviral combination therapy. JAMA 280(1):67–71

    Article  CAS  PubMed  Google Scholar 

  174. Schuetz TJ, Gallo GJ, Sheldon L, Tempst P, Kingston RE (1991) Isolation of a cDNA for HSF2: evidence for two heat shock factor genes in humans. Proc Natl Acad Sci U S A 88(16):6911–6915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Sen S, Deshmane SL, Kaminski R, Amini S, Datta PK (2017) Non-metabolic role of PKM2 in regulation of the HIV-1 LTR. J Cell Physiol 232(3):517–525

    Article  CAS  PubMed  Google Scholar 

  176. Serrao E, Wang CH, Frederick T, Lee CL, Anthony P, Arribas-Layton D, Baker K, Millstein J, Kovacs A, Neamati N (2014) Alteration of select gene expression patterns in individuals infected with HIV-1. J Med Virol 86(4):678–686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Shan L, Yang HC, Rabi SA, Bravo HC, Shroff NS, Irizarry RA, Zhang H, Margolick JB, Siliciano JD, Siliciano RF (2011) Influence of host gene transcription level and orientation on HIV-1 latency in a primary-cell model. J Virol 85(11):5384–5393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Shao J, Han B, Cao P, Zhang B, Liu M, Li D, Zhou N, Hao Q, Duan X, Chang Y, Nakai A, Fan Y, Tan K (2019) HSF1 phosphorylation by cyclosporin A confers hyperthermia sensitivity through suppression of HSP expression. Biochim Biophys Acta Gene Regul Mech 1862(8):846–857

    Article  CAS  PubMed  Google Scholar 

  179. Soltys BJ, Gupta RS (1996) Immunoelectron microscopic localization of the 60-kDa heat shock chaperonin protein (Hsp60) in mammalian cells. Exp Cell Res 222(1):16–27

    Article  CAS  PubMed  Google Scholar 

  180. Soncin F, Zhang X, Chu B, Wang X, Asea A, Ann Stevenson M, Sacks DB, Calderwood SK (2003) Transcriptional activity and DNA binding of heat shock factor-1 involve phosphorylation on threonine 142 by CK2. Biochem Biophys Res Commun 303(2):700–706

    Article  CAS  PubMed  Google Scholar 

  181. Sousa AI, Pinto VLJ (2016) Community viral load of HIV in Brazil, 2007 – 2011: potential impact of highly active antiretroviral therapy (HAART) in reducing new infections. Rev Bras Epidemiol 19(3):582–593

    Article  PubMed  Google Scholar 

  182. Speth C, Prohaszka Z, Mair M, Stockl G, Zhu X, Jobstl B, Fust G, Dierich MP (1999) A 60 kD heat-shock protein-like molecule interacts with the HIV transmembrane glycoprotein gp41. Mol Immunol 36(9):619–628

    Article  CAS  PubMed  Google Scholar 

  183. Stanley SK, Bressler PB, Poli G, Fauci AS (1990) Heat shock induction of HIV production from chronically infected promonocytic and T cell lines. J Immunol 145(4):1120–1126

    CAS  PubMed  Google Scholar 

  184. Sugiyama R, Naganuma H, Nishitsuji H, Takaku H (2011a) Human immunodeficiency virus-1 Nef suppresses Hsp70-mediated Tat activation. FEBS Lett 585(21):3367–3371

    Article  CAS  PubMed  Google Scholar 

  185. Sugiyama R, Nishitsuji H, Furukawa A, Katahira M, Habu Y, Takeuchi H, Ryo A, Takaku H (2011b) Heat shock protein 70 inhibits HIV-1 Vif-mediated ubiquitination and degradation of APOBEC3G. J Biol Chem 286(12):10051–10057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Sullivan EK, Weirich CS, Guyon JR, Sif S, Kingston RE (2001) Transcriptional activation domains of human heat shock factor 1 recruit human SWI/SNF. Mol Cell Biol 21(17):5826–5837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Sung JA, Sholtis K, Kirchherr J, Kuruc JD, Gay CL, Nordstrom JL, Bollard CM, Archin NM, Margolis DM (2017) Vorinostat renders the replication-competent latent reservoir of human immunodeficiency virus (HIV) vulnerable to clearance by CD8 T cells. EBioMedicine 23:52–58

    Article  PubMed  PubMed Central  Google Scholar 

  188. Swan CL, Evans TG, Sylvain N, Krone PH (2012) Zebrafish HSF4: a novel protein that shares features of both HSF1 and HSF4 of mammals. Cell Stress Chaperones 17(5):623–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Tanabe M, Nakai A, Kawazoe Y, Nagata K (1997) Different thresholds in the responses of two heat shock transcription factors, HSF1 and HSF3. J Biol Chem 272(24):15389–15395

    Article  CAS  PubMed  Google Scholar 

  190. Thielens NM, Bally IM, Ebenbichler CF, Dierich MP, Arlaud GJ (1993) Further characterization of the interaction between the C1q subcomponent of human C1 and the transmembrane envelope glycoprotein gp41 of HIV-1. J Immunol 151(11):6583–6592

    CAS  PubMed  Google Scholar 

  191. Tonkiss J, Calderwood SK (2005) Regulation of heat shock gene transcription in neuronal cells. Int J Hyperth 21(5):433–444

    Article  CAS  Google Scholar 

  192. Tristem M, Purvis A, Quicke DL (1998) Complex evolutionary history of primate lentiviral vpr genes. Virology 240(2):232–237

    Article  CAS  PubMed  Google Scholar 

  193. Tsai TT, Chen CL, Tsai CC, Lin CF (2017) Targeting heat shock factor 1 as an antiviral strategy against dengue virus replication in vitro and in vivo. Antivir Res 145:44–53

    Article  CAS  PubMed  Google Scholar 

  194. Tyagi M, Pearson RJ, Karn J (2010) Establishment of HIV latency in primary CD4+ cells is due to epigenetic transcriptional silencing and P-TEFb restriction. J Virol 84(13):6425–6437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  195. Vandamme AM, Van Vaerenbergh K, De Clercq E (1998) Anti-human immunodeficiency virus drug combination strategies. Antivir Chem Chemother 9(3):187–203

    Article  CAS  PubMed  Google Scholar 

  196. Verdin E, Paras P Jr, Van Lint C (1993) Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation. EMBO J 12(8):3249–3259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Vihervaara A, Sistonen L (2014) HSF1 at a glance. J Cell Sci 127(Pt 2):261–266

    Article  CAS  PubMed  Google Scholar 

  198. Vuister GW, Kim SJ, Orosz A, Marquardt J, Wu C, Bax A (1994) Solution structure of the DNA-binding domain of Drosophila heat shock transcription factor. Nat Struct Biol 1(9):605–614

    Article  CAS  PubMed  Google Scholar 

  199. Wang TY, Chen YM, Chen TY (2016) Molecular cloning of orange-spotted grouper (Epinephelus coioides) heat shock transcription factor 1 isoforms and characterization of their expressions in response to nodavirus. Fish Shellfish Immunol 59:123–136

    Article  CAS  PubMed  Google Scholar 

  200. Westerheide SD, Anckar J, Stevens SM Jr, Sistonen L, Morimoto RI (2009) Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323(5917):1063–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Williams SA, Greene WC (2007) Regulation of HIV-1 latency by T-cell activation. Cytokine 39(1):63–74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Williams SA, Chen LF, Kwon H, Fenard D, Bisgrove D, Verdin E, Greene WC (2004) Prostratin antagonizes HIV latency by activating NF-kappaB. J Biol Chem 279(40):42008–42017

    Article  CAS  PubMed  Google Scholar 

  203. Wyzewski Z, Gregorczyk KP, Szczepanowska J, Szulc-Dabrowska L (2018) Functional role of Hsp60 as a positive regulator of human viral infection progression. Acta Virol 62(1):33–40

    Article  CAS  PubMed  Google Scholar 

  204. Xia W, Voellmy R (1997) Hyperphosphorylation of heat shock transcription factor 1 is correlated with transcriptional competence and slow dissociation of active factor trimers. J Biol Chem 272(7):4094–4102

    Article  CAS  PubMed  Google Scholar 

  205. Xu D, Zalmas LP, La Thangue NB (2008) A transcription cofactor required for the heat-shock response. EMBO Rep 9(7):662–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Xu YM, Huang DY, Chiu JF, Lau AT (2012) Post-translational modification of human heat shock factors and their functions: a recent update by proteomic approach. J Proteome Res 11(5):2625–2634

    Article  CAS  PubMed  Google Scholar 

  207. Xue Y, Acar M (2018) Mechanisms for the epigenetic inheritance of stress response in single cells. Curr Genet 64(6):1221–1228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  208. Yamamoto N, Takemori Y, Sakurai M, Sugiyama K, Sakurai H (2009) Differential recognition of heat shock elements by members of the heat shock transcription factor family. FEBS J 276(7):1962–1974

    Article  CAS  PubMed  Google Scholar 

  209. Yang Y, Zhou Y, Xiong X, Huang M, Ying X, Wang M (2018) ALG3 is activated by heat shock factor 2 and promotes breast cancer growth. Med Sci Monit 24:3479–3487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. Yang LN, Ning ZY, Wang L, Yan X, Meng ZQ (2019) HSF2 regulates aerobic glycolysis by suppression of FBP1 in hepatocellular carcinoma. Am J Cancer Res 9(8):1607–1621

    CAS  PubMed  PubMed Central  Google Scholar 

  211. Zaikos TD, Painter MM, Sebastian Kettinger NT, Terry VH, Collins KL (2018) Class 1-selective histone deacetylase (HDAC) inhibitors enhance HIV latency reversal while preserving the activity of HDAC isoforms necessary for maximal HIV gene expression. J Virol 92(6)

    Google Scholar 

  212. Zanin-Zhorov A, Cahalon L, Tal G, Margalit R, Lider O, Cohen IR (2018) Heat shock protein 60 enhances CD4+CD25+ regulatory T cell function via innate TLR2 signaling. J Clin Invest 128(6):2651

    Article  PubMed  PubMed Central  Google Scholar 

  213. Zeng X, Pan X, Xu X, Lin J, Que F, Tian Y, Li L, Liu S (2017) Resveratrol reactivates latent HIV through increasing histone acetylation and activating heat shock factor 1. J Agric Food Chem 65(22):4384–4394

    Article  CAS  PubMed  Google Scholar 

  214. Zhang J, Goodson ML, Hong Y, Sarge KD (2008) MEL-18 interacts with HSF2 and the SUMO E2 UBC9 to inhibit HSF2 sumoylation. J Biol Chem 283(12):7464–7469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Zhao RY, Bukrinsky MI (2014) HIV-1 accessory proteins: VpR. Methods Mol Biol 1087:125–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Zhong YH, Cheng HZ, Peng H, Tang SC, Wang P (2016) Heat shock factor 2 is associated with the occurrence of lung cancer by enhancing the expression of heat shock proteins. Oncol Lett 12(6):5106–5112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  217. Zou J, Salminen WF, Roberts SM, Voellmy R (1998) Correlation between glutathione oxidation and trimerization of heat shock factor 1, an early step in stress induction of the Hsp response. Cell Stress Chaperones 3(2):130–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Authors thank Dr. Shibo Jiang at Fudan University, China, for providing the essential cell lines used in the experiment. This study was funded by Natural Science of China (grant number 31370781 and 81773787), the National S&T Key Special foundation (2014ZX09509001-004), the Natural Science Foundation of Guangdong Province (S201102005207) and National Science and Technology Major Project (2018ZX10301101).

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All authors declare they have no conflict of interest.

Ethical Approval for Studies Involving Humans

This article does not contain any studies with human participants performed by any of the authors.

Ethical Approval for Studies Involving Animals

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Xu, X., Pan, X., Liu, S. (2020). Role of Heat Shock Factor 1 in HIV. In: Asea, A.A.A., Kaur, P. (eds) Heat Shock Proteins in Inflammatory Diseases. Heat Shock Proteins, vol 22. Springer, Cham. https://doi.org/10.1007/7515_2020_11

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