Table Info

Table 1.

Cytoskeletal proteins interacting with HGAL

Protein symbol	Protein name
ACTG1	Actin, cytoplasmic 2
ADD3	Gamma-adducin
AFDN	Afadin
ALDH18A1	Delta-1-pyrroline-5-carboxylate synthase
ARHGAP25	Rho GTPase-activating protein 25
CCT2	T-complex protein 1 subunit beta
CCT7	T-complex protein 1 subunit eta
CLINT1	Clathrin interactor
CRKL	Crk-like protein
EHD1	EH domain-containing protein 1
EPB41L5	Band 4.1-like protein 5
EPS15	Epidermal growth factor receptor substrate 15
ERBIN	Erbin
EZR	Ezrin
GCSAM (HGAL)	GCSAM protein
MARK2	Serine/threonine-protein kinase MARK2
MSN	Moesin
PICALM	Phosphatidylinositol-binding clathrin assembly protein
PLEKHA5	Pleckstrin homology domain-containing family A member 5
PLS3	Plastin-3
PPFIBP1	Liprin-beta-1
SLC3A2	4F2 cell-surface antigen heavy chain
SNX1	Sorting nexin-1
SWAP70	Switch associated protein 70
TNS3	Tensin-3
TUBA1C	Tubulin alpha-1C chain
TUBA4A	Tubulin alpha-4A chain
TUBB	Tubulin beta chain
TUBB2B	Tubulin beta-2B chain
TUBB4B	Tubulin beta-4B chain
WASF2	Wiskott-Aldrich syndrome protein family member 2

Declarations

Acknowledgments

We thank to Sylvester Comprehensive Cancer Center for its continuous support over the years that included access to facilities and funding.

Author contributions

XJ and ISL: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing—original draft. ISL: Funding acquisition, Project administration, Resources, Supervision, Writing—review & editing.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent to publication

Not applicable.

Availability of data and materials

Not applicable.

Funding

ISL was approved by National Cancer Institute [1R01CA233945, U01CA195568], University of Miami SCCC (the Intramural Funding Program), Dwoskin and Anthony Rizzo Families Foundations and Jaime Erin Follicular Lymphoma Research Consortium. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright

References

Das B, Mitra P. Protein interaction network-based deep learning framework for identifying disease-associated human proteins. J Mol Biol. 2021;433:167149. [DOI] [PubMed]

Tomkins JE, Manzoni C. Advances in protein-protein interaction network analysis for Parkinson’s disease. Neurobiol Dis. 2021;155:105395. [DOI] [PubMed]

Zhong M, Lee GM, Sijbesma E, Ottmann C, Arkin MR. Modulating protein-protein interaction networks in protein homeostasis. Curr Opin Chem Biol. 2019;50:55–65. [DOI] [PubMed] [PMC]

Ichii M, Oritani K, Toda J, Hosen N, Matsuda T, Kanakura Y. Signal-transducing adaptor protein-1 and protein-2 in hematopoiesis and diseases. Exp Hematol. 2022;105:10–7. [DOI] [PubMed]

Matsuda T, Oritani K. STAP-2 adaptor protein regulates multiple steps of immune and inflammatory responses. Biol Pharm Bull. 2021;44:895–901. [DOI] [PubMed]

Wedegaertner H, Pan WA, Gonzalez CC, Gonzalez DJ, Trejo J. The α-arrestin ARRDC3 is an emerging multifunctional adaptor protein in cancer. Antioxid Redox Signal. 2022;36:1066–79. [DOI] [PubMed] [PMC]

Borah S, Bhowmick NA. The adaptor protein SHCA launches cancer invasion. J Biol Chem. 2020;295:10560–1. [DOI] [PubMed] [PMC]

Lin VT, Lin FT. TRIP6: an adaptor protein that regulates cell motility, antiapoptotic signaling and transcriptional activity. Cell Signal. 2011;23:1691–7. [DOI] [PubMed] [PMC]

Poosekeaw P, Pairojkul C, Sripa B, Sa Ngiamwibool P, Iamsaard S, Sakonsinsiri C, et al. Adaptor protein XB130 regulates the aggressiveness of cholangiocarcinoma. PLoS One. 2021;16:e0259075. [DOI] [PubMed] [PMC]

10.

Takayanagi H, Hayase J, Kamakura S, Miyano K, Chishiki K, Yuzawa S, et al. Intramolecular interaction in LGN, an adaptor protein that regulates mitotic spindle orientation. J Biol Chem. 2019;294:19655–66. [DOI] [PubMed] [PMC]

11.

Thompson BJ. Par-3 family proteins in cell polarity & adhesion. FEBS J. 2022;289:596–613. [DOI] [PubMed] [PMC]

12.

Wang J, Moerner WE, Shapiro L. A localized adaptor protein performs distinct functions at the Caulobacter cell poles. Proc Natl Acad Sci U S A. 2021;118:e2024705118. [DOI] [PubMed] [PMC]

13.

Luo W, Garcia-Gonzalez I, Fernández-Chacón M, Casquero-Garcia V, Sanchez-Muñoz MS, Mühleder S, et al. Arterialization requires the timely suppression of cell growth. Nature. 2021;589:437–41. [DOI] [PubMed] [PMC]

14.

Totaro A, Panciera T, Piccolo S. YAP/TAZ upstream signals and downstream responses. Nat Cell Biol. 2018;20:888–99. [DOI] [PubMed] [PMC]

15.

Wu X, Wang Y, Huang R, Gai Q, Liu H, Shi M, et al. SOSTDC1-producing follicular helper T cells promote regulatory follicular T cell differentiation. Science. 2020;369:984–8. [DOI] [PubMed]

16.

Mena EL, Jevtić P, Greber BJ, Gee CL, Lew BG, Akopian D, et al. Structural basis for dimerization quality control. Nature. 2020;586:452–6. [DOI] [PubMed] [PMC]

17.

Sharmeen N, Sulea T, Whiteway M, Wu C. The adaptor protein Ste50 directly modulates yeast MAPK signaling specificity through differential connections of its RA domain. Mol Biol Cell. 2019;30:794–807. [DOI] [PubMed] [PMC]

18.

Sluchanko NN, Bustos DM. Chapter two - Intrinsic disorder associated with 14-3-3 proteins and their partners. In: Uversky VN, editor. Dancing protein clouds: intrinsically disordered proteins in health and disease, part A. Academic Press; 2019. pp. 19–61. [DOI] [PubMed]

19.

Crilly SE, Ko W, Weinberg ZY, Puthenveedu MA. Conformational specificity of opioid receptors is determined by subcellular location irrespective of agonist. eLife. 2021;10:e67478. [DOI] [PubMed] [PMC]

20.

Eichel K, von Zastrow M. Subcellular organization of GPCR signaling. Trends Pharmacol Sci. 2018;39:200–8. [DOI] [PubMed] [PMC]

21.

Samson AL, Garnish SE, Hildebrand JM, Murphy JM. Location, location, location: a compartmentalized view of TNF-induced necroptotic signaling. Sci Signal. 2021;14:eabc6178. [DOI] [PubMed]

22.

Cancro MP, Tomayko MM. Memory B cells and plasma cells: the differentiative continuum of humoral immunity. Immunol Rev. 2021;303:72–82. [DOI] [PubMed]

23.

Elsner RA, Shlomchik MJ. Germinal center and extrafollicular B cell responses in vaccination, immunity, and autoimmunity. Immunity. 2020;53:1136–50. [DOI] [PubMed] [PMC]

24.

Gars E, Butzmann A, Ohgami R, Balakrishna JP, O’Malley DP. The life and death of the germinal center. Ann Diagn Pathol. 2020;44:151421. [DOI] [PubMed]

25.

Young C, Brink R. The unique biology of germinal center B cells. Immunity. 2021;54:1652–64. [DOI] [PubMed]

26.

Zhang Y, Garcia-Ibanez L, Toellner KM. Regulation of germinal center B-cell differentiation. Immunol Rev. 2016;270:8–19. Erratum in: Immunol Rev. 2016;272:202. [DOI] [PubMed] [PMC]

27.

Weinstock DM, Dalla-Favera R, Gascoyne RD, Leonard JP, Levy R, Lossos IS, et al. A roadmap for discovery and translation in lymphoma. Blood. 2015;125:2175–7. [DOI] [PubMed] [PMC]

28.

Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403:503–11. [DOI] [PubMed]

29.

Natkunam Y, Lossos IS, Taidi B, Zhao S, Lu X, Ding F, et al. Expression of the human germinal center-associated lymphoma (HGAL) protein, a new marker of germinal center B-cell derivation. Blood. 2005;105:3979–86. [DOI] [PubMed] [PMC]

30.

Xie X, Sundram U, Natkunam Y, Kohler S, Hoppe RT, Kim YH, et al. Expression of HGAL in primary cutaneous large B-cell lymphomas: evidence for germinal center derivation of primary cutaneous follicular lymphoma. Mod Pathol. 2008;21:653–9. [DOI] [PubMed]

31.

Koo M, Zhang J, Tan B, Kurzer J, Gratzinger D, Zhao S, et al. Human germinal center-associated lymphoma (HGAL) is a reliable marker of normal and neoplastic follicular helper T cells including angioimmunoblastic T-Cell lymphoma. Am J Surg Pathol. 2022;46:643–54. [DOI] [PubMed]

32.

Pan Z, Shen Y, Du C, Zhou G, Rosenwald A, Staudt LM, et al. Two newly characterized germinal center B-cell-associated genes, GCET1 and GCET2, have differential expression in normal and neoplastic B cells. Am J Pathol. 2003;163:135–44. [DOI] [PubMed] [PMC]

33.

Lossos C, Bayraktar S, Weinzierl E, Younes SF, Hosein PJ, Tibshirani RJ, et al. LMO2 and BCL6 are associated with improved survival in primary central nervous system lymphoma. Br J Haematol. 2014;165:640–8. [DOI] [PubMed] [PMC]

34.

Lossos IS, Alizadeh AA, Rajapaksa R, Tibshirani R, Levy R. HGAL is a novel interleukin-4-inducible gene that strongly predicts survival in diffuse large B-cell lymphoma. Blood. 2003;101:433–40. [DOI] [PubMed]

35.

Azambuja D, Lossos IS, Biasoli I, Morais JC, Britto L, Scheliga A, et al. Human germinal center-associated lymphoma protein expression is associated with improved failure-free survival in Brazilian patients with classical Hodgkin lymphoma. Leuk Lymphoma. 2009;50:1830–6. [DOI] [PubMed] [PMC]

36.

Natkunam Y, Hsi ED, Aoun P, Zhao S, Elson P, Pohlman B, et al. Expression of the human germinal center-associated lymphoma (HGAL) protein identifies a subset of classic Hodgkin lymphoma of germinal center derivation and improved survival. Blood. 2007;109:298–305. [DOI] [PubMed] [PMC]

37.

Schenten D, Egert A, Pasparakis M, Rajewsky K. M17, a gene specific for germinal center (GC) B cells and a prognostic marker for GC B-cell lymphomas, is dispensable for the GC reaction in mice. Blood. 2006;107:4849–56. [DOI] [PubMed] [PMC]

38.

Davis RE, Ngo VN, Lenz G, Tolar P, Young RM, Romesser PB, et al. Chronic active B-cell-receptor signalling in diffuse large B-cell lymphoma. Nature. 2010;463:88–92. [DOI] [PubMed] [PMC]

39.

Humphrey MB, Lanier LL, Nakamura MC. Role of ITAM-containing adapter proteins and their receptors in the immune system and bone. Immunol Rev. 2005;208:50–65. [DOI] [PubMed]

40.

Monroe JG. ITAM-mediated tonic signalling through pre-BCR and BCR complexes. Nat Rev Immunol. 2006;6:283–94. [DOI] [PubMed]

41.

Jelinek DF. Regulation of B lymphocyte differentiation. Ann Allergy Asthma Immunol. 2000;84:375–85. [DOI] [PubMed]

42.

Turqueti-Neves A, Otte M, Prazeres da Costa O, Höpken UE, Lipp M, Buch T, et al. B-cell-intrinsic STAT6 signaling controls germinal center formation. Eur J Immunol. 2014;44:2130–8. [DOI] [PubMed]

43.

Cubedo E, Maurin M, Jiang X, Lossos IS, Wright KL. PRDM1/Blimp1 downregulates expression of germinal center genes LMO2 and HGAL. FEBS J. 2011;278:3065–75. [DOI] [PubMed] [PMC]

44.

Angelin-Duclos C, Cattoretti G, Chang DH, Lin KI, Lin Y, Yu J, et al. Role of B-lymphocyte-induced maturation protein-1 in terminal differentiation of B cells and other cell lineages. Cold Spring Harb Symp Quant Biol. 1999;64:61–70. [DOI] [PubMed]

45.

Kuo TC, Calame KL. B lymphocyte-induced maturation protein (Blimp)-1, IFN regulatory factor (IRF)-1, and IRF-2 can bind to the same regulatory sites¹. J Immunol. 2004;173:5556–63. [DOI] [PubMed]

46.

Mandelbaum J, Bhagat G, Tang H, Mo T, Brahmachary M, Shen Q, et al. BLIMP1 is a tumor suppressor gene frequently disrupted in activated B cell-like diffuse large B cell lymphoma. Cancer Cell. 2010;18:568–79. [DOI] [PubMed] [PMC]

47.

Pasqualucci L, Compagno M, Houldsworth J, Monti S, Grunn A, Nandula SV, et al. Inactivation of the PRDM1/BLIMP1 gene in diffuse large B cell lymphoma. J Exp Med. 2006;203:311–7. [DOI] [PubMed] [PMC]

48.

Guo F, Luo Y, Jiang X, Lu X, Roberti D, Lossos C, et al. Recent BCR stimulation induces a negative autoregulatory loop via FBXO10 mediated degradation of HGAL. Leukemia. 2020;34:553–66. [DOI] [PubMed]

49.

Dagan LN, Jiang X, Bhatt S, Cubedo E, Rajewsky K, Lossos IS. miR-155 regulates HGAL expression and increases lymphoma cell motility. Blood. 2012;119:513–20. [DOI] [PubMed] [PMC]

50.

Basso K, Schneider C, Shen Q, Holmes AB, Setty M, Leslie C, et al. BCL6 positively regulates AID and germinal center gene expression via repression of miR-155. J Exp Med. 2012;209:2455–65. [DOI] [PubMed] [PMC]

51.

Sun W, Zhang L, Lin L, Wang W, Ge Y, Liu Y, et al. Chronic psychological stress impairs germinal center response by repressing miR-155. Brain Behav Immun. 2019;76:48–60. [DOI] [PubMed]

52.

Thai TH, Calado DP, Casola S, Ansel KM, Xiao C, Xue Y, et al. Regulation of the germinal center response by microRNA-155. Science. 2007;316:604–8. [DOI] [PubMed]

53.

Munch-Petersen HD, Ralfkiaer U, Sjö LD, Hother C, Asmar F, Nielsen BS, et al. Differential expression of miR-155 and miR-21 in tumor and stroma cells in diffuse large B-cell lymphoma. Appl Immunohistochem Mol Morphol. 2015;23:188–95. [DOI] [PubMed]

54.

Yim RL, Wong KY, Kwong YL, Loong F, Leung CY, Chu R, et al. Methylation of miR-155-3p in mantle cell lymphoma and other non-Hodgkin’s lymphomas. Oncotarget. 2014;5:9770–82. [DOI] [PubMed] [PMC]

55.

Lu X, Sicard R, Jiang X, Stockus JN, McNamara G, Abdulreda M, et al. HGAL localization to cell membrane regulates B-cell receptor signaling. Blood. 2015;125:649–57. [DOI] [PubMed] [PMC]

56.

Jiang X, Lu X, McNamara G, Liu X, Cubedo E, Sarosiek KA, et al. HGAL, a germinal center specific protein, decreases lymphoma cell motility by modulation of the RhoA signaling pathway. Blood. 2010;116:5217–27. [DOI] [PubMed] [PMC]

57.

Romero-Camarero I, Jiang X, Natkunam Y, Lu X, Vicente-Dueñas C, Gonzalez-Herrero I, et al. Germinal centre protein HGAL promotes lymphoid hyperplasia and amyloidosis via BCR-mediated Syk activation. Nat Commun. 2013;4:1338. [DOI] [PubMed] [PMC]

58.

Jiang X, Lu X, Zhang Y, Lacaria L, Schuchardt BJ, Mikles DC, et al. Interplay between HGAL and Grb2 proteins regulates B-cell receptor signaling. Blood Adv. 2019;3:2286–97. [DOI] [PubMed] [PMC]

59.

Grucza RA, Bradshaw JM, Mitaxov V, Waksman G. Role of electrostatic interactions in SH2 domain recognition: salt-dependence of tyrosyl-phosphorylated peptide binding to the tandem SH2 domain of the Syk kinase and the single SH2 domain of the Src kinase†. Biochemistry. 2000;39:10072–81. [DOI] [PubMed]

60.

Hughes CE, Finney BA, Koentgen F, Lowe KL, Watson SP. The N-terminal SH2 domain of Syk is required for (hem)ITAM, but not integrin, signaling in mouse platelets. Blood. 2015;125:144–54. [DOI] [PubMed] [PMC]

61.

Hosoe Y, Numoto N, Inaba S, Ogawa S, Morii H, Abe R, et al. Structural and functional properties of Grb2 SH2 dimer in CD28 binding. Biophys Physicobiol. 2019;16:80–8. [DOI] [PubMed] [PMC]

62.

Sanches K, Dias RVR, da Silva PH, Fossey MA, Caruso ÍP, de Souza FP, et al. Grb2 dimer interacts with Coumarin through SH2 domains: a combined experimental and molecular modeling study. Heliyon. 2019;5:e02869. [DOI] [PubMed] [PMC]

63.

Jang IK, Cronshaw DG, Xie LK, Fang G, Zhang J, Oh H, et al. Growth-factor receptor-bound protein-2 (Grb2) signaling in B cells controls lymphoid follicle organization and germinal center reaction. Proc Natl Acad Sci U S A. 2011;108:7926–31. [DOI] [PubMed] [PMC]

64.

Pan Z, Shen Y, Ge B, Du C, McKeithan T, Chan WC. Studies of a germinal centre B-cell expressed gene, GCET2, suggest its role as a membrane associated adapter protein. Br J Haematol. 2007;137:578–90. [DOI] [PubMed] [PMC]

65.

Cho KO, Hunt CA, Kennedy MB. The rat brain postsynaptic density fraction contains a homolog of the drosophila discs-large tumor suppressor protein. Neuron. 1992;9:929–42. [DOI] [PubMed]

66.

Cowburn D. Peptide recognition by PTB and PDZ domains. Curr Opin Struct Biol. 1997;7:835–8. [DOI] [PubMed]

67.

O’Connor K, Chen M. Dynamic functions of RhoA in tumor cell migration and invasion. Small GTPases. 2013;4:141–7. [DOI] [PubMed] [PMC]

68.

Wang B, Dai T, Sun W, Wei Y, Ren J, Zhang L, et al. Protein N-myristoylation: functions and mechanisms in control of innate immunity. Cell Mol Immunol. 2021;18:878–88. [DOI] [PubMed] [PMC]

69.

Jin J, Zhi X, Wang X, Meng D. Protein palmitoylation and its pathophysiological relevance. J Cell Physiol. 2021;236:3220–33. [DOI] [PubMed]

70.

Bonilla FA, Oettgen HC. Adaptive immunity. J Allergy Clin Immunol. 2010;125:S33–40. [DOI] [PubMed]

71.

Kitamura D, Roes J, Kühn R, Rajewsky K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin μ chain gene. Nature. 1991;350:423–6. [DOI] [PubMed]

72.

Reichlin A, Hu Y, Meffre E, Nagaoka H, Gong S, Kraus M, et al. B cell development is arrested at the immature B cell stage in mice carrying a mutation in the cytoplasmic domain of immunoglobulin β. J Exp Med. 2001;193:13–23. [DOI] [PubMed] [PMC]

73.

Tanaka S, Baba Y. B cell receptor signaling. In: Wang JY, editor. B cells in immunity and tolerance. Singapore: Springer; 2020. pp. 23–36. [DOI] [PubMed]

74.

Treanor B. B-cell receptor: from resting state to activate. Immunology. 2012;136:21–7. [DOI] [PubMed] [PMC]

75.

Küppers R. Mechanisms of B-cell lymphoma pathogenesis. Nat Rev Cancer. 2005;5:251–62. [DOI] [PubMed]

76.

Smith SH, Reth M. Perspectives on the nature of BCR-mediated survival signals. Mol Cell. 2004;14:696–7. [DOI] [PubMed]

77.

Kuokkanen E, Šuštar V, Mattila PK. Molecular control of B cell activation and immunological synapse formation. Traffic. 2015;16:311–26. [DOI] [PubMed]

78.

Fhu CW, Ali A. Protein lipidation by palmitoylation and myristoylation in cancer. Front Cell Dev Biol. 2021;9:673647. [DOI] [PubMed] [PMC]

79.

Martin DD, Beauchamp E, Berthiaume LG. Post-translational myristoylation: fat matters in cellular life and death. Biochimie. 2011;93:18–31. [DOI] [PubMed]

80.

Belov AA, Mohammadi M. Grb2, a double-edged sword of receptor tyrosine kinase signaling. Sci Signal. 2012;5:pe49. [DOI] [PubMed] [PMC]

81.

Tari AM, Lopez-Berestein G. GRB2: a pivotal protein in signal transduction. Semin Oncol. 2001;28:142–7. [DOI] [PubMed]

82.

Manno B, Oellerich T, Schnyder T, Corso J, Lösing M, Neumann K, et al. The Dok-3/Grb2 adaptor module promotes inducible association of the lipid phosphatase SHIP with the BCR in a coreceptor-independent manner. Eur J Immunol. 2016;46:2520–30. [DOI] [PubMed]

83.

Schnyder T, Castello A, Feest C, Harwood NE, Oellerich T, Urlaub H, et al. B cell receptor-mediated antigen gathering requires ubiquitin ligase Cbl and adaptors Grb2 and Dok-3 to recruit dynein to the signaling microcluster. Immunity. 2011;34:905–18. [DOI] [PubMed]

84.

Iber D. Formation of the B cell synapse: retention or recruitment? Cell Mol Life Sci. 2005;62:206–13. [DOI] [PubMed]

85.

Ford WL. Lymphocyte migration and immune responses. Prog Allergy. 1975;19:1–59. [DOI] [PubMed]

86.

Germain RN, Robey EA, Cahalan MD. A decade of imaging cellular motility and interaction dynamics in the immune system. Science. 2012;336:1676–81. [DOI] [PubMed] [PMC]

87.

Drillenburg P, Pals ST. Cell adhesion receptors in lymphoma dissemination. Blood. 2000;95:1900–10. [DOI] [PubMed]

88.

Pals ST, de Gorter DJ, Spaargaren M. Lymphoma dissemination: the other face of lymphocyte homing. Blood. 2007;110:3102–11. [DOI] [PubMed]

89.

Wickramarachchi DC, Theofilopoulos AN, Kono DH. Immune pathology associated with altered actin cytoskeleton regulation. Autoimmunity. 2010;43:64–75. [DOI] [PubMed] [PMC]

90.

Papa R, Penco F, Volpi S, Gattorno M. Actin remodeling defects leading to autoinflammation and immune dysregulation. Front Immunol. 2021;11:604206. [DOI] [PubMed] [PMC]

91.

Sancho D, Vicente-Manzanares M, Mittelbrunn M, Montoya MC, Gordón-Alonso M, Serrador JM, et al. Regulation of microtubule-organizing center orientation and actomyosin cytoskeleton rearrangement during immune interactions. Immunol Rev. 2002;189:84–97. [DOI] [PubMed]

92.

Fife CM, McCarroll JA, Kavallaris M. Movers and shakers: cell cytoskeleton in cancer metastasis. Br J Pharmacol. 2014;171:5507–23. Erratum in: Br J Pharmacol. 2017;174:116. [DOI] [PubMed] [PMC]

93.

Hall A. The cytoskeleton and cancer. Cancer Metastasis Rev. 2009;28:5–14. [DOI] [PubMed]

94.

Sprenkeler EGG, Webbers SDS, Kuijpers TW. When actin is not actin’ like it should: a new category of distinct primary immunodeficiency disorders. J Innate Immun. 2021;13:3–25. [DOI] [PubMed] [PMC]

95.

Healy JA, Nugent A, Rempel RE, Moffitt AB, Davis NS, Jiang X, et al. GNA13 loss in germinal center B cells leads to impaired apoptosis and promotes lymphoma in vivo. Blood. 2016;127:2723–31. [DOI] [PubMed] [PMC]

96.

Muppidi JR, Schmitz R, Green JA, Xiao W, Larsen AB, Braun SE, et al. Loss of signalling via Gα13 in germinal centre B-cell-derived lymphoma. Nature. 2014;516:254–8. [DOI] [PubMed] [PMC]

97.

Victora GD, Schwickert TA, Fooksman DR, Kamphorst AO, Meyer-Hermann M, Dustin ML, et al. Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell. 2010;143:592–605. [DOI] [PubMed] [PMC]

98.

Cyster JG, Allen CDC. B cell responses: cell interaction dynamics and decisions. Cell. 2019;177:524–40. [DOI] [PubMed] [PMC]

99.

Cyster JG, Schwab SR. Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu Rev Immunol. 2012;30:69–94. [DOI] [PubMed]

100.

Arnon TI, Cyster JG. Blood, sphingosine-1-phosphate and lymphocyte migration dynamics in the spleen. In: Oldstone MBA, Rosen H, editors. Sphingosine-1-phosphate signaling in immunology and infectious diseases. Cham: Springer International Publishing; 2014. pp. 107–28. [DOI] [PubMed]

101.

Bannard O, Cyster JG. Germinal centers: programmed for affinity maturation and antibody diversification. Curr Opin Immunol. 2017;45:21–30. [DOI] [PubMed]

102.

Green JA, Cyster JG. S1PR2 links germinal center confinement and growth regulation. Immunol Rev. 2012;247:36–51. [DOI] [PubMed] [PMC]

103.

Lu X, Chen J, Malumbres R, Cubedo Gil E, Helfman DM, Lossos IS. HGAL, a lymphoma prognostic biomarker, interacts with the cytoskeleton and mediates the effects of IL-6 on cell migration. Blood. 2007;110:4268–77. [DOI] [PubMed] [PMC]

104.

Lu Y, Kwan AH, Trewhella J, Jeffries CM. The C0C1 fragment of human cardiac myosin binding protein C has common binding determinants for both actin and myosin. J Mol Biol. 2011;413:908–13. [DOI] [PubMed]

105.

Jiang X, Lu X, Gentles AJ, Zhao D, Wander SA, Zhang Y, et al. HGAL inhibits lymphoma dissemination by interacting with multiple cytoskeletal proteins. Blood Adv. 2021;5:5072–85. [DOI] [PubMed] [PMC]

106.

Squire J. Special issue: the actin-myosin interaction in muscle: background and overview. Int J Mol Sci. 2019;20:5715. [DOI] [PubMed] [PMC]

107.

Guhathakurta P, Prochniewicz E, Thomas DD. Actin-myosin interaction: structure, function and drug discovery. Int J Mol Sci. 2018;19:2628. [DOI] [PubMed] [PMC]

108.

Finley NL, Cuperman TI. Cardiac myosin binding protein-C: a structurally dynamic regulator of myocardial contractility. Pflugers Arch. 2014;466:433–8. [DOI] [PubMed]

109.

Wang JC, Yim YI, Wu X, Jaumouille V, Cameron A, Waterman CM, et al. A B-cell actomyosin arc network couples integrin co-stimulation to mechanical force-dependent immune synapse formation. eLife. 2022;11:e72805. [DOI] [PubMed] [PMC]

110.

Hall A. Rho family GTPases. Biochem Soc Trans. 2012;40:1378–82. [DOI] [PubMed]

111.

Hodge RG, Ridley AJ. Regulating Rho GTPases and their regulators. Nat Rev Mol Cell Biol. 2016;17:496–510. [DOI] [PubMed]

112.

Choi EK, Kim JG, Kim HJ, Cho JY, Jeong H, Park Y, et al. Regulation of RhoA GTPase and novel target proteins for ROCK. Small GTPases. 2020;11:95–102. [DOI] [PubMed] [PMC]

113.

Kim JG, Islam R, Cho JY, Jeong H, Cap KC, Park Y, et al. Regulation of RhoA GTPase and various transcription factors in the RhoA pathway. J Cell Physiol. 2018;233:6381–92. [DOI] [PubMed]

114.

Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol. 2009;10:778–90. [DOI] [PubMed] [PMC]

115.

Conti MA, Even-Ram S, Liu C, Yamada KM, Adelstein RS. Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice^*. J Biol Chem. 2004;279:41263–6. [DOI] [PubMed]

116.

Ma X, Bao J, Adelstein RS. Loss of cell adhesion causes hydrocephalus in nonmuscle myosin II-B-ablated and mutated mice. Mol Biol Cell. 2007;18:2305–12. [DOI] [PubMed] [PMC]

117.

Girkontaite I, Missy K, Sakk V, Harenberg A, Tedford K, Pötzel T, et al. Lsc is required for marginal zone B cells, regulation of lymphocyte motility and immune responses. Nat Immunol. 2001;2:855–62. [DOI] [PubMed]

118.

Roux KJ, Kim DI, Raida M, Burke B. A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J Cell Biol. 2012;196:801–10. [DOI] [PubMed] [PMC]

119.

Kim DI, Jensen SC, Noble KA, Kc B, Roux KH, Motamedchaboki K, et al. An improved smaller biotin ligase for BioID proximity labeling. Mol Biol Cell. 2016;27:1188–96. [DOI] [PubMed] [PMC]

120.

Baecklund E, Natkunam Y, Backlin C, Iliadou A, Askling J, Ekbom A, et al. Expression of the human germinal-centre-associated lymphoma protein in diffuse large B-cell lymphomas in patients with rheumatoid arthritis. Br J Haematol. 2008;141:69–72. [DOI] [PubMed]

121.

Reddy A, Zhang J, Davis NS, Moffitt AB, Love CL, Waldrop A, et al. Genetic and functional drivers of diffuse large B cell lymphoma. Cell. 2017;171:481–94.e15. [DOI] [PubMed] [PMC]

122.

McKinney M, Moffitt AB, Gaulard P, Travert M, De Leval L, Nicolae A, et al. The genetic basis of hepatosplenic T-cell lymphoma. Cancer Discov. 2017;7:369–79. [DOI] [PubMed] [PMC]

123.

Lossos IS. BLIMP1 against lymphoma: the verdict is reached. Cancer Cell. 2010;18:537–9. [DOI] [PubMed]

124.

Calado DP, Zhang B, Srinivasan L, Sasaki Y, Seagal J, Unitt C, et al. Constitutive canonical NF-κB activation cooperates with disruption of BLIMP1 in the pathogenesis of activated B cell-like diffuse large cell lymphoma. Cancer Cell. 2010;18:580–9. [DOI] [PubMed] [PMC]

125.

Raboso-Gallego J, Casado-García A, Jiang X, Isidro-Hernández M, Gentles AJ, Zhao S, et al. Conditional expression of HGAL leads to the development of diffuse large B-cell lymphoma in mice. Blood. 2021;137:1741–53. [DOI] [PubMed] [PMC]