Activation of the complement cascade enhances motility of leukemic cells by downregulating expression of HO-1

Leukemia

Volumn 31, Issue 2, 2017, Pages 446-458

  Abdelbaset Ismail, A ^a   Borkowska Rzeszotek, S ^b   Kubis, E ^b   Bujko, K ^a   Brzezniakiewicz Janus K ^c   Bolkun, L ^d   Kloczko, J ^d   Moniuszko, M ^d   Basak, G W ^e   Wiktor Jedrzejczak, W ^e   Ratajczak, M Z ^a,e  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b POMERANIAN MEDICAL UNIVERSITY   (Poland)

^c Multispecialist Hospital   (Poland)

^d MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

^e MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C5A RECEPTOR; FIBRONECTIN; HEME OXYGENASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; PROTEIN KINASE B; PROTEIN P42; PROTEIN P44; SHORT HAIRPIN RNA; STROMAL CELL DERIVED FACTOR 1; CD33 ANTIGEN; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C5; SMALL INTERFERING RNA;

ACUTE MYELOID LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER IMMUNOLOGY; CANCER PATIENT; CELL ADHESION; CELL MIGRATION; CHEMOTAXIS; CHRONIC MYELOID LEUKEMIA; CLINICAL ARTICLE; CLONOGENIC ASSAY; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; DOWN REGULATION; ENZYME REGULATION; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HEMATOPOIETIC CELL; HL-60 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; K-562 CELL LINE; LEUKEMIA CELL; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; U-937 CELL LINE; UPREGULATION; XENOTRANSPLANTATION; ANIMAL; CELL MOTION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; HEMATOPOIETIC STEM CELL; IMMUNOLOGY; IMMUNOPHENOTYPING; LEUKEMIA; METABOLISM; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOTAXIS; COMPLEMENT ACTIVATION; COMPLEMENT C3; COMPLEMENT C5; DOWN-REGULATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, LEUKEMIC; GENE KNOCKOUT TECHNIQUES; HEMATOPOIETIC STEM CELLS; HEME OXYGENASE-1; HETEROGRAFTS; HUMANS; IMMUNOPHENOTYPING; LEUKEMIA; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEOLYSIS; RECEPTOR, ANAPHYLATOXIN C5A; RNA, SMALL INTERFERING; SIALIC ACID BINDING IG-LIKE LECTIN 3; SIGNAL TRANSDUCTION;

EID: 84983468735     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2016.198     Document Type: Article

References (60)

1. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 2010; 11: 785-797.
2. Amara U, Flierl MA, Rittirsch D, Klos A, Chen H, Acker B et al. Molecular intercommunication between the complement and coagulation systems. J Immunol 2010; 185: 5628-5636.
3. Kozarcanin H, Lood C, Munthe-Fog L, Sandholm K, Hamad OA, Bengtsson AA et al. The lectin complement pathway serine proteases (MASPs) represent a possible crossroad between the coagulation and complement systems in thromboinflammation. J Thromb Haemost 2016; 14: 531-545.
4. Schraufstatter IU, Discipio RG, Zhao M, Khaldoyanidi SK. C3a and C5a are chemotactic factors for human mesenchymal stem cells, which cause prolonged ERK1/2 phosphorylation. J Immunol 2009; 182: 3827-3836.
5. Schraufstatter IU, Khaldoyanidi SK, DiScipio RG. Complement activation in the context of stem cells and tissue repair. World J Stem Cells 2015; 7: 1090-1108.
6. Reca R, Mastellos D, Majka M, Marquez L, Ratajczak J, Franchini S et al. Functional receptor for C3a anaphylatoxin is expressed by normal hematopoietic stem/progenitor cells, and C3a enhances their homing-related responses to SDF-1. Blood 2003; 101: 3784-3793.
7. Ratajczak J, Reca R, Kucia M, Majka M, Allendorf DJ, Baran JT et al. Mobilization studies in mice deficient in either C3 or C3a receptor (C3aR) reveal a novel role for complement in retention of hematopoietic stem/progenitor cells in bone marrow. Blood 2004; 103: 2071-2078.
8. Ratajczak MZ, Reca R, Wysoczynski M, Kucia M, Baran JT, Allendorf DJ et al. Transplantation studies in C3-deficient animals reveal a novel role of the third complement component (C3) in engraftment of bone marrow cells. Leukemia 2004; 18: 1482-1490.
9. Lee HM, Wu W, Wysoczynski M, Liu R, Zuba-Surma EK, Kucia M et al. Impaired mobilization of hematopoietic stem/progenitor cells in C5-deficient mice supports the pivotal involvement of innate immunity in this process and reveals novel promobilization effects of granulocytes. Leukemia 2009; 23: 2052-2062.
10. Ratajczak MZ. A novel view of the adult bone marrow stem cell hierarchy and stem cell trafficking. Leukemia 2015; 29: 776-782.
11. Ratajczak MZ, Kim CH, Wojakowski W, Janowska-Wieczorek A, Kucia M, Ratajczak J. Innate immunity as orchestrator of stem cell mobilization. Leukemia 2010; 24: 1667-1675.
12. Bonig H, Papayannopoulou T. Hematopoietic stem cell mobilization: updated conceptual renditions. Leukemia 2013; 27: 24-31.
13. Lapidot T, Kollet O. The brain-bone-blood triad: traffic lights for stem-cell homing and mobilization. Hematology Am Soc Hematol Educ Program 2010; 2010: 1-6.
14. Lévesque JP, Helwani FM, Winkler IG. The endosteal 'osteoblastic' niche and its role in hematopoietic stem cell homing and mobilization. Leukemia 2010; 24: 1979-1992.
15. Mantel CR, O'Leary HA, Chitteti BR, Huang X, Cooper S, Hangoc G et al. Enhancing hematopoietic stem cell transplantation efficacy by mitigating oxygen shock. Cell 2015; 161: 1553-1565.
16. Levesque JP, Liu F, Simmons PJ, Betsuyaku T, Senior RM, Pham C et al. Characterization of hematopoietic progenitor mobilization in proteasedeficient mice. Blood 2004; 104: 65-72.
17. Adamiak M, Poniewierska-Baran A, Borkowska S, Schneider G, Abdelbaset-Ismail A, Suszynska M et al. Evidence that a lipolytic enzyme-hematopoieticspecific phospholipase C-beta2-promotes mobilization of hematopoietic stem cells by decreasing their lipid raft-mediated bone marrow retention and increasing the promobilizing effects of granulocytes. Leukemia 2016; 30: 919-928.
18. Imamura T, Yamamoto-Ibusuki M, Sueta A, Kubo T, Irie A, Kikuchi K et al. Influence of the C5a-C5a receptor system on breast cancer progression and patient prognosis. Breast Cancer 2015; e-pub ahead of print 22 October 2015.
19. Mikesch JH, Buerger H, Simon R, Brandt B. Decay-accelerating factor (CD55): a versatile acting molecule in human malignancies. Biochim Biophys Acta 2006; 1766: 42-52.
20. Kim KB, Yi JS, Nguyen N, Lee JH, Kwon YC, Ahn BY et al. Cell-surface receptor for complement component C1q (gC1qR) is a key regulator for lamellipodia formation and cancer metastasis. J Biol Chem 2011; 286: 23093-23101.
21. Ouyang Q, Zhang L, Jiang Y, Ni X, Chen S, Ye F et al. The membrane complement regulatory protein CD59 promotes tumor growth and predicts poor prognosis in breast cancer. Int J Oncol 2016; 48: 2015-2024.
22. Corrales L, Ajona D, Rafail S, Lasarte JJ, Riezu-Boj JI, Lambris JD et al. Anaphylatoxin C5a creates a favorable microenvironment for lung cancer progression. J Immunol 2012; 189: 4674-4683.
23. Cai K, Wan Y, Wang Z, Wang Y, Zhao X, Bao X. C5a promotes the proliferation of human nasopharyngeal carcinoma cells through PCAF-mediated STAT3 acetylation. Oncol Rep 2014; 32: 2260-2266.
24. Maeda Y, Kawano Y, Wada Y, Yatsuda J, Motoshima T, Murakami Y et al. C5aR is frequently expressed in metastatic renal cell carcinoma and plays a crucial role in cell invasion via the ERK and PI3 kinase pathways. Oncol Rep 2015; 33: 1844-1850.
25. Nunez-Cruz S, Gimotty PA, Guerra MW, Connolly DC, Wu YQ, DeAngelis RA et al. Genetic and pharmacologic inhibition of complement impairs endothelial cell function and ablates ovarian cancer neovascularization. Neoplasia 2012; 14: 994-1004.
26. Piao C, Cai L, Qiu S, Jia L, Song W, Du J. Complement 5a enhances hepatic metastases of colon cancer via monocyte chemoattractant protein-1-mediated inflammatory cell infiltration. J Biol Chem 2015; 290: 10667-10676.
27. Vadrevu SK, Chintala NK, Sharma SK, Sharma P, Cleveland C, Riediger L et al. Complement c5a receptor facilitates cancer metastasis by altering T-cell responses in the metastatic niche. Cancer Res 2014; 74: 3454-3465.
28. Nitta H, Wada Y, Kawano Y, Murakami Y, Irie A, Taniguchi K et al. Enhancement of human cancer cell motility and invasiveness by anaphylatoxin C5a via aberrantly expressed C5a receptor (CD88). Clin Cancer Res 2013; 19: 2004-2013.
29. Boulay F, Mery L, Tardif M, Brouchon L, Vignais P. Expression cloning of a receptor for C5a anaphylatoxin on differentiated HL-60 cells. Biochemistry 1991; 30: 2993-2999.
30. Burg M, Martin U, Bock D, Rheinheimer C, Kohl J, Bautsch W et al. Differential regulation of the C3a and C5a receptors (CD88) by IFN-gamma and PMA in U937 cells and related myeloblastic cell lines. J Immunol 1996; 157: 5574-5581.
31. Crass T, Raffetseder U, Martin U, Grove M, Klos A, Kohl J et al. Expression cloning of the human C3a anaphylatoxin receptor (C3aR) from differentiated U-937 cells. Eur J Immunol 1996; 26: 1944-1950.
32. Perianayagam MC, Madias NE, Pereira BJ, Jaber BL. CREB transcription factor modulates Bcl2 transcription in response to C5a in HL-60-derived neutrophils. Eur J Clin Invest 2006; 36: 353-361.
33. Rubin J, Titus L, Nanes MS. Regulation of complement 5a receptor expression in U937 cells by phorbol ester. J Leukoc Biol 1991; 50: 502-508.
34. Zahn S, Zwirner J, Spengler HP, Gotze O. Chemoattractant receptors for interleukin-8 and C5a: expression on peripheral blood leukocytes and differential regulation on HL-60 and AML-193 cells by vitamin D3 and all-trans retinoic acid. Eur J Immunol 1997; 27: 935-940.
35. Wysoczynski M, Ratajczak J, Pedziwiatr D, Rokosh G, Bolli R, Ratajczak MZ. Identification of heme oxygenase 1 (HO-1) as a novel negative regulator of mobilization of hematopoietic stem/progenitor cells. Stem Cell Rev 2015; 11: 110-118.
36. Abdelbaset-Ismail A, Borkowska S, Janowska-Wieczorek A, Tonn T, Rodriguez C, Moniuszko M et al. Novel evidence that pituitary gonadotropins directly stimulate human leukemic cells-studies of myeloid cell lines and primary patient AML and CML cells. Oncotarget 2016; 7: 3033-3046.
37. Freitas A, Alves-Filho JC, Secco DD, Neto AF, Ferreira SH, Barja-Fidalgo C et al. Heme oxygenase/carbon monoxid-biliverdin pathway down regulates neutrophil rolling, adhesion and migration in acute inflammation. Br J Pharmacol 2006; 149: 345-354.
38. Wysoczynski M, Reca R, Lee H, Wu W, Ratajczak J, Ratajczak MZ. Defective engraftment of C3aR-/- hematopoietic stem progenitor cells shows a novel role of the C3a-C3aR axis in bone marrow homing. Leukemia 2009; 23: 1455-1461.
39. Ratajczak MZ, Adamiak M. Membrane lipid rafts, master regulators of hematopoietic stem cell retention in bone marrow and their trafficking. Leukemia 2015; 29: 1452-1457.
40. Petrie RJ, Doyle AD, Yamada KM. Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 2009; 10: 538-549.
41. Pio R, Ajona D, Lambris JD. Complement inhibition in cancer therapy. Semin Immunol 2013; 25: 54-64.
42. Markiewski MM, DeAngelis RA, Benencia F, Ricklin-Lichtsteiner SK, Koutoulaki A, Gerard C et al. Modulation of the antitumor immune response by complement. Nat Immunol 2008; 9: 1225-1235.
43. Adamiak M, Iv JB, Zhao J, Abdelbaset-Ismail A, Grubczak K, Borkowska S et al. Downregulation of heme oxygenase 1 (HO-1) activity in hematopoietic cells enhances their engraftment after transplantation. Cell Transplant 2016; 25: 1265-1276.
44. Naidu S, Vijayan V, Santoso S, Kietzmann T, Immenschuh S. Inhibition and genetic deficiency of p38 MAPK up-regulates heme oxygenase-1 gene expression via Nrf2. J Immunol 2009; 182: 7048-7057.
45. Honczarenko M, Ratajczak MZ, Nicholson-Weller A, Silberstein LE. Complement C3a enhances CXCL12 (SDF-1)-mediated chemotaxis of bone marrow hematopoietic cells independently of C3a receptor. J Immunol 2005; 175: 3698-3706.
46. Camous L, Roumenina L, Bigot S, Brachemi S, Fremeaux-Bacchi V, Lesavre P et al. Complement alternative pathway acts as a positive feedback amplification of neutrophil activation. Blood 2011; 117: 1340-1349.
47. Sadik CD, Kim ND, Luster AD. Neutrophils cascading their way to inflammation. Trends Immunol 2011; 32: 452-460.
48. Price PJ, Banki Z, Scheideler A, Stoiber H, Verschoor A, Sutter G et al. Complement component C5 recruits neutrophils in the absence of C3 during respiratory infection with modified vaccinia virus Ankara. J Immunol 2015; 194: 1164-1168.
49. Gutzmer R, Lisewski M, Zwirner J, Mommert S, Diesel C, Wittmann M et al. Human monocyte-derived dendritic cells are chemoattracted to C3a after up-regulation of the C3a receptor with interferons. Immunology 2004; 111: 435-443.
50. Kim CH, Wu W, Wysoczynski M, Abdel-Latif A, Sunkara M, Morris A et al. Conditioning for hematopoietic transplantation activates the complement cascade and induces a proteolytic environment in bone marrow: a novel role for bioactive lipids and soluble C5b-C9 as homing factors. Leukemia 2012; 26: 106-116.
51. Flierl MA, Rittirsch D, Nadeau BA, Day DE, Zetoune FS, Sarma JV et al. Functions of the complement components C3 and C5 during sepsis. FASEB J 2008; 22: 3483-3490.
52. Rutkowski MJ, Sughrue ME, Kane AJ, Mills SA, Parsa AT. Cancer and the complement cascade. Mol Cancer Res 2010; 8: 1453-1465.
53. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 2010; 80: 1895-1903.
54. Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, Atkinson MA et al. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 2004; 165: 1045-1053.
55. Radhakrishnan N, Yadav SP, Sachdeva A, Pruthi PK, Sawhney S, Piplani T et al. Human heme oxygenase-1 deficiency presenting with hemolysis, nephritis, and asplenia. J Pediatr Hematol Oncol 2011; 33: 74-78.
56. Keum YS, Yu S, Chang PP, Yuan X, Kim JH, Xu C et al. Mechanism of action of sulforaphane: inhibition of p38 mitogen-activated protein kinase isoforms contributing to the induction of antioxidant response element-mediated heme oxygenase-1 in human hepatoma HepG2 cells. Cancer Res 2006; 66: 8804-8813.
57. Ganan-Gomez I, Bohannan ZS, Garcia-Manero G. p38 MAPK in MDS. Aging (Albany NY) 2015; 7: 346-347.
58. Sjoberg AP, Trouw LA, Blom AM. Complement activation and inhibition: a delicate balance. Trends Immunol 2009; 30: 83-90.
59. Morgan J, Spendlove I, Durrant LG. The role of CD55 in protecting the tumour environment from complement attack. Tissue Antigens 2002; 60: 213-223.
60. Liu J, Miwa T, Hilliard B, Chen Y, Lambris JD, Wells AD et al. The complement inhibitory protein DAF (CD55) suppresses T cell immunity in vivo. J Exp Med 2005; 201: 567-577.