Skip to main content

Sumoylation as an Integral Mechanism in Bacterial Infection and Disease Progression

  • Chapter
  • First Online:
SUMO Regulation of Cellular Processes

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 963))

Abstract

Post translational modification pathways regulate fundamental processes of cells and thus govern vital functions. Among these, particularly the modification with Small Ubiquitin-like Modifiers (SUMO) is being recognized as a pathway crucial for cell homeostasis and health. Understandably, bacterial pathogens intervene with the SUMO pathway of the host for ensuring successful infection. Among the bacterial pathogens known to target host sumoylation varied points of intervention are utilized. Majority of them including Salmonella Typhimurium, Shigella flexneri and Listeria monocytogenes target the E2 conjugating enzyme Ubc9. While others, such as Xanthomonase compestris, target the desumoylation machineries mimicking cysteine protease activity. Still others such as Ehrlichia chaffeensis and Anaplasma phagocytophilum utilize host SUMO-machinery for sumoylating their own effectors. Together such changes lead to modulation of host proteome and transcriptome thereby leading to major alterations in signal transduction that favor invasion and bacterial multiplication. Such interplay between bacterial pathogens and host sumoylation has added a new dimension to host-pathogen biology and its understanding could be vital for developing potential therapeutic intervention strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ashida H, Kim M, Schmidt-Supprian M, Ma A, Ogawa M, Sasakawa C (2010) A bacterial E3 ubiquitin ligase IpaH9.8 targets NEMO/IKKgamma to dampen the host NF-kappaB-mediated inflammatory response. Nat Cell Biol 12:66–73

    Article  CAS  PubMed  Google Scholar 

  • Beyer AR, Truchan HK, May LJ, Walker NJ, Borjesson DL, Carlyon JA (2015) The Anaplasma phagocytophilum effector AmpA hijacks host cell SUMOylation. Cell Microbiol 17:504–519

    Article  CAS  PubMed  Google Scholar 

  • Bohren KM, Nadkarni V, Song JH, Gabbay KH, Owerbach D (2004) A M55 V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J Biol Chem 279:27233–27238

    Article  CAS  PubMed  Google Scholar 

  • Bossis G, Malnou CE, Farras R, Andermarcher E, Hipskind R, Rodriguez M, Schmidt D, Muller S, Jariel-Encontre I, Piechaczyk M (2005) Down-regulation of c-Fos/c-Jun AP-1 dimer activity by sumoylation. Mol Cell Biol 25:6964–6979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burns KE, Liu WT, Boshoff HI, Dorrestein PC, Barry CE 3rd (2009) Proteasomal protein degradation in Mycobacteria is dependent upon a prokaryotic ubiquitin-like protein. J Biol Chem 284:3069–3075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burns KE, Cerda-Maira FA, Wang T, Li H, Bishai WR, Darwin KH (2010) “Depupylation” of prokaryotic ubiquitin-like protein from mycobacterial proteasome substrates. Mol Cell 39:821–827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Solomon WC, Kang Y, Cerda-Maira F, Darwin KH, Walters KJ (2009) Prokaryotic ubiquitin-like protein pup is intrinsically disordered. J Mol Biol 392:208–217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chosed R, Tomchick DR, Brautigam CA, Mukherjee S, Negi VS, Machius M, Orth K (2007) Structural analysis of Xanthomonas XopD provides insights into substrate specificity of ubiquitin-like protein proteases. J Biol Chem 282:6773–6782

    Article  CAS  PubMed  Google Scholar 

  • Cimarosti H, Ashikaga E, Jaafari N, Dearden L, Rubin P, Wilkinson KA, Henley JM (2012) Enhanced SUMOylation and SENP-1 protein levels following oxygen and glucose deprivation in neurones. J. Cerebral Blood Flow Metab. 32:17–22

    Article  CAS  Google Scholar 

  • Cougnoux A, Dalmasso G, Martinez R, Buc E, Delmas J, Gibold L, Sauvanet P, Darcha C, Dechelotte P, Bonnet M, Pezet D, Wodrich H, Darfeuille-Michaud A, Bonnet R (2014) Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype. Gut 63:1932–1942

    Article  CAS  PubMed  Google Scholar 

  • Cubenas-Potts C, Matunis MJ (2013) SUMO: a multifaceted modifier of chromatin structure and function. Dev Cell 24:1–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dal PM, van der Goot FG (2016) Pore-forming toxins: ancient, but never really out of fashion. Nat Rev Microbiol 14:77–92

    Google Scholar 

  • Dalmasso G, Cougnoux A, Delmas J, Darfeuille-Michaud A, Bonnet R (2014) The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment. Gut Microbes 5:675–680

    Article  PubMed  PubMed Central  Google Scholar 

  • Darwin KH, Ehrt S, Gutierrez-Ramos JC, Weich N, Nathan CF (2003) The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302:1963–1966

    Article  CAS  PubMed  Google Scholar 

  • Datwyler AL, Lattig-Tunnemann G, Yang W, Paschen W, Lee SL, Dirnagl U, Endres M, Harms C (2011) SUMO2/3 conjugation is an endogenous neuroprotective mechanism. J Cereb Blood Flow Metab 31:2152–2159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desterro JM, Rodriguez MS, Hay RT (1998) SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol Cell 2:233–239

    Article  CAS  PubMed  Google Scholar 

  • Dunphy PS, Luo T, McBride JW (2014) Ehrlichia chaffeensis exploits host SUMOylation pathways to mediate effector-host interactions and promote intracellular survival. Infect Immun 82:4154–4168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Eifler K, Vertegaal AC (2015) SUMOylation-mediated regulation of cell cycle progression and cancer. Trends Biochem Sci 40:779–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisenreich W, Dandekar T, Heesemann J, Goebel W (2010) Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat Rev Microbiol 8:401–412

    Article  CAS  PubMed  Google Scholar 

  • Everett RD, Boutell C, Hale BG (2013) Interplay between viruses and host sumoylation pathways. Nat Rev Microbiol 11:400–411

    Article  CAS  PubMed  Google Scholar 

  • Eylert E, Schar J, Mertins S, Stoll R, Bacher A, Goebel W, Eisenreich W (2008) Carbon metabolism of Listeria monocytogenes growing inside macrophages. Mol Microbiol 69:1008–1017

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Walsh CA (2004) The many faces of filamin: a versatile molecular scaffold for cell motility and signalling. Nat Cell Biol 6:1034–1038

    Article  CAS  PubMed  Google Scholar 

  • Flotho A, Melchior F (2013) Sumoylation: a regulatory protein modification in health and disease. Annu Rev Biochem 82:357–385

    Article  CAS  PubMed  Google Scholar 

  • Fritah S, Lhocine N, Golebiowski F, Mounier J, Andrieux A, Jouvion G, Hay RT, Sansonetti P, Dejean A (2014) Sumoylation controls host anti-bacterial response to the gut invasive pathogen Shigella flexneri. EMBO Rep 15:965–972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gandotra S, Schnappinger D, Monteleone M, Hillen W, Ehrt S (2007) In vivo gene silencing identifies the Mycobacterium tuberculosis proteasome as essential for the bacteria to persist in mice. Nat Med 13:1515–1520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gartner A, Muller S (2014) PML, SUMO, and RNF4: guardians of nuclear protein quality. Mol Cell 55:1–3

    Article  PubMed  CAS  Google Scholar 

  • Golebiowski F, Matic I, Tatham MH, Cole C, Yin Y, Nakamura A, Cox J, Barton GJ, Mann M, Hay RT (2009) System-wide changes to SUMO modifications in response to heat shock. Sci Signal 2:ra24

    Article  PubMed  CAS  Google Scholar 

  • Grice EA, Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9:244–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grice EA, Segre JA (2012) The human microbiome: our second genome. Annu Rev Genomics Hum Genet 13:151–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo C, Henley JM (2014) Wrestling with stress: roles of protein SUMOylation and deSUMOylation in cell stress response. IUBMB Life 66:71–77

    Article  CAS  PubMed  Google Scholar 

  • Guo L, Giasson BI, Glavis-Bloom A, Brewer MD, Shorter J, Gitler AD, Yang X (2014) A cellular system that degrades misfolded proteins and protects against neurodegeneration. Mol Cell 55:15–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hannemann S, Gao B, Galan JE (2013) Salmonella modulation of host cell gene expression promotes its intracellular growth. PLoS Pathog 9:e1003668

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hannich JT, Lewis A, Kroetz MB, Li SJ, Heide H, Emili A, Hochstrasser M (2005) Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J Biol Chem 280:4102–4110

    Article  CAS  PubMed  Google Scholar 

  • Hay RT (2005) SUMO: a history of modification. Mol Cell 18:1–12

    Article  CAS  PubMed  Google Scholar 

  • Hickey CM, Wilson NR, Hochstrasser M (2012) Function and regulation of SUMO proteases. Nat Rev Mol Cell Biol 13:755–766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hilgarth RS, Murphy LA, Skaggs HS, Wilkerson DC, Xing H, Sarge KD (2004) Regulation and function of SUMO modification. J Biol Chem 279:53899–53902

    Article  CAS  PubMed  Google Scholar 

  • Hoefer J, Schafer G, Klocker H, Erb HH, Mills IG, Hengst L, Puhr M, Culig Z (2012) PIAS1 is increased in human prostate cancer and enhances proliferation through inhibition of p21. Am J Pathol 180:2097–2107

    Article  CAS  PubMed  Google Scholar 

  • Hong B, Wang L, Lammertyn E, Geukens N, Van Mellaert L, Li Y, Anne J (2005) Inactivation of the 20S proteasome in Streptomyces lividans and its influence on the production of heterologous proteins. Microbiology 151:3137–3145

    Article  CAS  PubMed  Google Scholar 

  • Hong Y, Xing X, Li S, Bi H, Yang C, Zhao F, Liu Y, Ao X, Chang AK, Wu H (2011) SUMOylation of DEC1 protein regulates its transcriptional activity and enhances its stability. PloS One 6:e23046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hotson A, Chosed R, Shu H, Orth K, Mudgett MB (2003) Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol Microbiol 50:377–389

    Article  CAS  PubMed  Google Scholar 

  • Huang TT, Wuerzberger-Davis SM, Wu ZH, Miyamoto S (2003) Sequential modification of NEMO/IKKgamma by SUMO-1 and ubiquitin mediates NF-kappaB activation by genotoxic stress. Cell 115:565–576

    Article  CAS  PubMed  Google Scholar 

  • Imkamp F, Striebel F, Sutter M, Ozcelik D, Zimmermann N, Sander P, Weber-Ban E (2010) Dop functions as a depupylase in the prokaryotic ubiquitin-like modification pathway. EMBO Rep 11:791–797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isberg RR, Barnes P (2001) Subversion of integrins by enteropathogenic Yersinia. J Cell Sci 114:21–28

    CAS  PubMed  Google Scholar 

  • Iyer LM, Burroughs AM, Aravind L (2008) Unraveling the biochemistry and provenance of pupylation: a prokaryotic analog of ubiquitination. Biol Direct 3:45

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kaiko GE, Stappenbeck TS (2014) Host-microbe interactions shaping the gastrointestinal environment. Trends Immunol 35:538–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kessler JD, Kahle KT, Sun T, Meerbrey KL, Schlabach MR, Schmitt EM, Skinner SO, Xu Q, Li MZ, Hartman ZC, Rao M, Yu P, Dominguez-Vidana R, Liang AC, Solimini NL, Bernardi RJ, Yu B, Hsu T, Golding I, Luo J, Osborne CK, Creighton CJ, Hilsenbeck SG, Schiff R, Shaw CA, Elledge SJ, Westbrook TF (2012) A SUMOylation-dependent transcriptional subprogram is required for Myc-driven tumorigenesis. Science 335:348–353

    Article  CAS  PubMed  Google Scholar 

  • Kim JG, Stork W, Mudgett MB (2013) Xanthomonas type III effector XopD desumoylates tomato transcription factor SlERF4 to suppress ethylene responses and promote pathogen growth. Cell Host Microbe 13:143–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knipfer N, Shrader TE (1997) Inactivation of the 20S proteasome in Mycobacterium smegmatis. Mol Microbiol 25:375–383

    Article  CAS  PubMed  Google Scholar 

  • Kurihara I, Shibata H, Kobayashi S, Suda N, Ikeda Y, Yokota K, Murai A, Saito I, Rainey WE, Saruta T (2005) Ubc9 and protein inhibitor of activated STAT 1 activate chicken ovalbumin upstream promoter-transcription factor I-mediated human CYP11B2 gene transcription. J Biol Chem 280:6721–6730

    Article  CAS  PubMed  Google Scholar 

  • Lamichhane G, Raghunand TR, Morrison NE, Woolwine SC, Tyagi S, Kandavelou K, Bishai WR (2006) Deletion of a Mycobacterium tuberculosis proteasomal ATPase homologue gene produces a slow-growing strain that persists in host tissues. J Infect Dis 194:1233–1240

    Article  CAS  PubMed  Google Scholar 

  • Lee YJ, Hallenbeck JM (2013) SUMO and ischemic tolerance. NeuroMolecular Med 15:771–781

    Article  CAS  PubMed  Google Scholar 

  • Lee PS, Chang C, Liu D, Derynck R (2003) Sumoylation of Smad4, the common Smad mediator of transforming growth factor-beta family signaling. J Biol Chem 278:27853–27863

    Article  CAS  PubMed  Google Scholar 

  • Lee YJ, Miyake S, Wakita H, McMullen DC, Azuma Y, Auh S, Hallenbeck JM (2007) Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. J. Cerebral Blood Flow Metab. 27:950–962

    Article  CAS  Google Scholar 

  • Lee YJ, Mou Y, Maric D, Klimanis D, Auh S, Hallenbeck JM (2011) Elevated global SUMOylation in Ubc9 transgenic mice protects their brains against focal cerebral ischemic damage. PloS One 6:e25852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li SJ, Hochstrasser M (1999) A new protease required for cell-cycle progression in yeast. Nature 398:246–251

    Article  CAS  PubMed  Google Scholar 

  • Liang YC, Lee CC, Yao YL, Lai CC, Schmitz ML, Yang WM (2016) SUMO5, a novel poly-SUMO isoform, regulates PML nuclear bodies. Sci Rep 6:26509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao S, Shang Q, Zhang X, Zhang J, Xu C, Tu X (2009) Pup, a prokaryotic ubiquitin-like protein, is an intrinsically disordered protein. Biochem J 422:207–215

    Article  CAS  PubMed  Google Scholar 

  • Liu LB, Omata W, Kojima I, Shibata H (2007) The SUMO conjugating enzyme Ubc9 is a regulator of GLUT4 turnover and targeting to the insulin-responsive storage compartment in 3 T3-L1 adipocytes. Diabetes 56:1977–1985

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Bridges R, Wortham A, Kulesz-Martin M (2012) NF-kappaB repression by PIAS3 mediated RelA SUMOylation. PloS One 7:e37636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mabb AM, Miyamoto S (2007) SUMO and NF-kappaB ties. Cell Mol Life Sci 64:1979–1996

    Article  CAS  PubMed  Google Scholar 

  • Marx J (2005) Cell biology. SUMO wrestles its way to prominence in the cell. Science 307:836–839

    Article  CAS  PubMed  Google Scholar 

  • Matsuda S, Adachi J, Ihara M, Tanuma N, Shima H, Kakizuka A, Ikura M, Ikura T, Matsuda T (2016) Nuclear pyruvate kinase M2 complex serves as a transcriptional coactivator of arylhydrocarbon receptor. Nucleic Acids Res 44:636–647

    Article  CAS  PubMed  Google Scholar 

  • Mesquita FS, Thomas M, Sachse M, Santos AJ, Figueira R, Holden DW (2012) The Salmonella deubiquitinase SseL inhibits selective autophagy of cytosolic aggregates. PLoS Pathog 8:e1002743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao J, Niu J, Wang K, Xiao Y, Du Y, Zhou L, Duan L, Li S, Yang G, Chen L, Tong M, Miao Y (2014) Heat shock factor 2 levels are associated with the severity of ulcerative colitis. PloS One 9:e88822

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miller MR, White A, Boots M (2005) The evolution of host resistance: tolerance and control as distinct strategies. J Theor Biol 236:198–207

    Article  CAS  PubMed  Google Scholar 

  • Miller MJ, Barrett-Wilt GA, Hua Z, Vierstra RD (2010) Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis. Proc Natl Acad Sci U S A 107:16512–16517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mo YY, Yu Y, Theodosiou E, Ee PL, Beck WT (2005) A role for Ubc9 in tumorigenesis. Oncogene 24:2677–2683

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee S, Keitany G, Li Y, Wang Y, Ball HL, Goldsmith EJ, Orth K (2006) Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312:1211–1214

    Article  CAS  PubMed  Google Scholar 

  • Muller S, Berger M, Lehembre F, Seeler JS, Haupt Y, Dejean A (2000) c-Jun and p53 activity is modulated by SUMO-1 modification. J Biol Chem 275:13321–13329

    Article  CAS  PubMed  Google Scholar 

  • Nuro-Gyina PK, Parvin JD (2016) Roles for SUMO in pre-mRNA processing. RNA 7:105–112

    CAS  PubMed  Google Scholar 

  • Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, Bliska JB, Mangel WF, Staskawicz B, Dixon JE (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290:1594–1597

    Article  CAS  PubMed  Google Scholar 

  • Ozcelik D, Barandun J, Schmitz N, Sutter M, Guth E, Damberger FF, Allain FH, Ban N, Weber-Ban E (2012) Structures of Pup ligase PafA and depupylase Dop from the prokaryotic ubiquitin-like modification pathway. Nat Commun 3:1014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pascual G, Fong AL, Ogawa S, Gamliel A, Li AC, Perissi V, Rose DW, Willson TM, Rosenfeld MG, Glass CK (2005) A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature 437:759–763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pearce MJ, Mintseris J, Ferreyra J, Gygi SP, Darwin KH (2008) Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science 322:1104–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribet D, Cossart P (2010) Pathogen-mediated posttranslational modifications: a re-emerging field. Cell 143:694–702

    Article  CAS  PubMed  Google Scholar 

  • Ribet D, Hamon M, Gouin E, Nahori MA, Impens F, Neyret-Kahn H, Gevaert K, Vandekerckhove J, Dejean A, Cossart P (2010) Listeria monocytogenes impairs SUMOylation for efficient infection. Nature 464:1192–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roden J, Eardley L, Hotson A, Cao Y, Mudgett MB (2004) Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells. Mol Plant-Microbe Interact 17:633–643

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez MS, Dargemont C, Hay RT (2001) SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J Biol Chem 276:12654–12659

    Article  CAS  PubMed  Google Scholar 

  • Roy BA, Kirchner JW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51–63

    Article  CAS  PubMed  Google Scholar 

  • Sampson DA, Wang M, Matunis MJ (2001) The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J Biol Chem 276:21664–21669

    Article  CAS  PubMed  Google Scholar 

  • Sansonetti P (2002) Host-pathogen interactions: the seduction of molecular cross talk. Gut 50(Suppl 3):III2–III8

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sathyan KM, Shen Z, Tripathi V, Prasanth KV, Prasanth SG (2011) A BEN-domain-containing protein associates with heterochromatin and represses transcription. J Cell Sci 124:3149–3163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seeler JS, Dejean A (2003) Nuclear and unclear functions of SUMO. Nat Rev Mol Cell Biol 4:690–699

    Article  CAS  PubMed  Google Scholar 

  • Sidik SM, Salsman J, Dellaire G, Rohde JR (2015) Shigella infection interferes with SUMOylation and increases PML-NB number. PloS One 10:e0122585

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smet-Nocca C, Wieruszeski JM, Leger H, Eilebrecht S, Benecke A (2011) SUMO-1 regulates the conformational dynamics of thymine-DNA Glycosylase regulatory domain and competes with its DNA binding activity. BMC Biochem 12:4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stindt MH, Carter S, Vigneron AM, Ryan KM, Vousden KH (2011) MDM2 promotes SUMO-2/3 modification of p53 to modulate transcriptional activity. Cell Cycle 10:3176–3188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Striebel F, Imkamp F, Sutter M, Steiner M, Mamedov A, Weber-Ban E (2009) Bacterial ubiquitin-like modifier Pup is deamidated and conjugated to substrates by distinct but homologous enzymes. Nat Struct Mol Biol 16:647–651

    Article  CAS  PubMed  Google Scholar 

  • Sutter M, Striebel F, Damberger FF, Allain FH, Weber-Ban E (2009) A distinct structural region of the prokaryotic ubiquitin-like protein (Pup) is recognized by the N-terminal domain of the proteasomal ATPase Mpa. FEBS Lett 583:3151–3157

    Article  CAS  PubMed  Google Scholar 

  • Tempe D, Vives E, Brockly F, Brooks H, De Rossi S, Piechaczyk M, Bossis G (2014) SUMOylation of the inducible (c-Fos:c-Jun)/AP-1 transcription complex occurs on target promoters to limit transcriptional activation. Oncogene 33:921–927

    Article  CAS  PubMed  Google Scholar 

  • Thomas M, Mesquita FS, Holden DW (2012) The DUB-ious lack of ALIS in Salmonella infection: a Salmonella deubiquitinase regulates the autophagy of protein aggregates. Autophagy 8:1824–1826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uemura A, Taniguchi M, Matsuo Y, Oku M, Wakabayashi S, Yoshida H (2013) UBC9 regulates the stability of XBP1, a key transcription factor controlling the ER stress response. Cell Struct Funct 38:67–79

    Article  CAS  PubMed  Google Scholar 

  • van Valen L (1973) A new evolutionary law. Evol Theory 1:1–30

    Google Scholar 

  • Venteclef N, Jakobsson T, Ehrlund A, Damdimopoulos A, Mikkonen L, Ellis E, Nilsson LM, Parini P, Janne OA, Gustafsson JA, Steffensen KR, Treuter E (2010) GPS2-dependent corepressor/SUMO pathways govern anti-inflammatory actions of LRH-1 and LXRbeta in the hepatic acute phase response. Genes Dev 24:381–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verma S, Mohapatra G, Ahmad SM, Rana S, Jain S, Khalsa JK, Srikanth CV (2015) Salmonella engages host microRNAs to modulate SUMOylation: a new arsenal for intracellular survival. Mol Cell Biol 35:2932–2946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vertegaal AC, Andersen JS, Ogg SC, Hay RT, Mann M, Lamond AI (2006) Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol Cell Proteomics 5:2298–2310

    Article  CAS  PubMed  Google Scholar 

  • Wade WG (2013) The oral microbiome in health and disease. Pharmacol Res 69:137–143

    Article  CAS  PubMed  Google Scholar 

  • Wang XD, Gong Y, Chen ZL, Gong BN, Xie JJ, Zhong CQ, Wang QL, Diao LH, Xu A, Han J, Altman A, Li Y (2015) TCR-induced sumoylation of the kinase PKC-theta controls T cell synapse organization and T cell activation. Nat Immunol 16:1195–1203

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson KA, Henley JM (2010) Mechanisms, regulation and consequences of protein SUMOylation. Biochem J 428:133–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang W, Sheng H, Warner DS, Paschen W (2008a) Transient focal cerebral ischemia induces a dramatic activation of small ubiquitin-like modifier conjugation. J. Cerebral Blood Flow Metab. 28:892–896

    Article  CAS  Google Scholar 

  • Yang W, Sheng HX, Warner DS, Paschen W (2008b) Transient global cerebral ischemia induces a massive increase in protein sumoylation. J Cereb Blood Flow Metab 28:269–279

    Article  PubMed  CAS  Google Scholar 

  • Yates G, Srivastava AK, Sadanandom A (2016) SUMO proteases: uncovering the roles of deSUMOylation in plants. J Exp Bot 67:2541–2548

    Article  CAS  PubMed  Google Scholar 

  • Yeh ET (2009) SUMOylation and De-SUMOylation: wrestling with life’s processes. J Biol Chem 284:8223–8227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YG, Wu S, Xia Y, Chen D, Petrof EO, Claud EC, Hsu W, Sun J (2012) Axin1 prevents Salmonella invasiveness and inflammatory response in intestinal epithelial cells. PloS One 7:e34942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou H, Monack DM, Kayagaki N, Wertz I, Yin J, Wolf B, Dixit VM (2005) Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-kappa B activation. J Exp Med 202:1327–1332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu S, Sachdeva M, Wu F, Lu Z, Mo YY (2010) Ubc9 promotes breast cell invasion and metastasis in a sumoylation-independent manner. Oncogene 29:1763–1772

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

CVS is a recipient of DBT-Wellcome Trust fellowship and core funding from UNESCO-Regional Centre for Biotechnology, Faridabad, India. SV was a Young Investigator awardee at Regional Centre for Biotechnology, Faridabad during the preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chittur V. Srikanth .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Srikanth, C.V., Verma, S. (2017). Sumoylation as an Integral Mechanism in Bacterial Infection and Disease Progression. In: Wilson, V. (eds) SUMO Regulation of Cellular Processes. Advances in Experimental Medicine and Biology, vol 963. Springer, Cham. https://doi.org/10.1007/978-3-319-50044-7_22

Download citation

Publish with us

Policies and ethics