Store-operated Ca2+ entry mediated regulation of polarization in differentiated human neutrophil-like HL-60 cells under hypoxia

Ma,Shuang; Cai,Chunqing; Ma,Yan; Bai,Zhengzhong; Meng,Xiaojing; Yang,Xinyi; Zou,Fei; Ge,Rili

doi:10.3892/mmr.2014.1894

Store-operated Ca2+ entry mediated regulation of polarization in differentiated human neutrophil-like HL-60 cells under hypoxia

Authors:
- Shuang Ma
- Chunqing Cai
- Yan Ma
- Zhengzhong Bai
- Xiaojing Meng
- Xinyi Yang
- Fei Zou
- Rili Ge
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Affiliations: Research Centre for High Altitude Medicine, Qinghai University Medical College, Qinghai University, Xining, Qinghai 810000, P.R. China, Department of Occupational Health and Occupational Medicine, School of Public Health and Tropical Medicine, Southern Medical University, Guangzhou, Guangdong 510515, P.R. China
Published online on: January 13, 2014 https://doi.org/10.3892/mmr.2014.1894
Pages: 819-824

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Abstract

The regulation of neutrophil polarization by calcium entry is critical for maintaining an effective host response. Hypoxia has a major effect on the apoptosis of neutrophils, however the role of store-operated Ca2+ entry (SOCE) in neutrophil polarization under hypoxia remains to be elucidated. In the present study, we examined the polarization of differentiated human neutrophil-like HL-60 (dHL-60) cells exposed to hypoxia (3% O2) and the results demonstrated that the percentage of polarized cells following exposure to an N-formyl-Met-Leu-Phe (fMLP) gradient in the Zigmond chamber was increased. We examined stromal interaction molecule 1 (STIM1) and Orai1 expression in dHL-60 cells during hypoxia, and it was observed that the expression of STIM1 and Orai1 was significantly reduced at day 2. However, no apparent change was observed on the first day, indicating that this effect is dependent on stimulation time. Fluo-4/acetoxymethyl (AM) ester imaging also demonstrated that SOCE was decreased in dHL-60 cells. The plasmid overexpression assay demonstrated that the response of polarization was returned to the control level. We demonstrated the inhibitory role of SOCE on the polarization of dHL-60 cells under hypoxic conditions, which may be the mechanism for the adaptation of neutrophils to hypoxia. SOCE is also suggested to be a key modulator of immune deficiency under hypoxic conditions and is potentially a therapeutic target.

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1	Eltzschig HK, Thompson LF, Karhausen J, et al: Endogenous adenosine produced during hypoxia attenuates neutrophil accumulation: coordination by extracellular nucleotide metabolism. Blood. 104:3986–3992. 2004. View Article : Google Scholar
2	Thompson AA, Binham J, Plant T, Whyte MK and Walmsley SR: Hypoxia, the HIF pathway and neutrophilic inflammatory responses. Biol Chem. 394:471–477. 2013. View Article : Google Scholar : PubMed/NCBI
3	Walmsley SR, Print C, Farahi N, et al: Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J Exp Med. 201:105–115. 2005. View Article : Google Scholar : PubMed/NCBI
4	Onsum M and Rao CV: A mathematical model for neutrophil gradient sensing and polarization. PLoS Comput Biol. 3:e362007. View Article : Google Scholar : PubMed/NCBI
5	O’Donnell NG, McSharry CP, Wilkinson PC and Asbury AJ: Comparison of the inhibitory effect of propofol, thiopentone and midazolam on neutrophil polarization in vitro in the presence or absence of human serum albumin. Br J Anaesth. 69:70–74. 1992.PubMed/NCBI
6	Allen DB, Maguire JJ, Mahdavian M, et al: Wound hypoxia and acidosis limit neutrophil bacterial killing mechanisms. Arch Surg. 132:991–996. 1997. View Article : Google Scholar : PubMed/NCBI
7	Jönsson K, Hunt TK and Mathes SJ: Oxygen as an isolated variable influences resistance to infection. Ann Surg. 208:783–787. 1988.PubMed/NCBI
8	Krupina TN, Korotaev MM, Pukhova IaI, Tsyganova NI and Likhacheva NP: Comparative evaluation of studies of the action of different levels of hypoxia on the human immunobiological status. Kosm Biol Aviakosm Med. 11:38–43. 1977.(In Russian).
9	Rotstein OD, Fiegel VD, Simmons RL and Knighton DR: The deleterious effect of reduced pH and hypoxia on neutrophil migration in vitro. J Surg Res. 45:298–303. 1988. View Article : Google Scholar : PubMed/NCBI
10	McGovern NN, Cowburn AS, Porter L, et al: Hypoxia selectively inhibits respiratory burst activity and killing of Staphylococcus aureus in human neutrophils. J Immunol. 186:453–463. 2011. View Article : Google Scholar
11	Marks PW and Maxfield FR: Transient increases in cytosolic free calcium appear to be required for the migration of adherent human neutrophils. J Cell Biol. 110:43–52. 1990.
12	Meshulam T, Proto P, Diamond RD and Melnick DA: Calcium modulation and chemotactic response: divergent stimulation of neutrophil chemotaxis and cytosolic calcium response by the chemotactic peptide receptor. J Immunol. 137:1954–1960. 1986.
13	Pettit EJ and Fay FS: Cytosolic free calcium and the cytoskeleton in the control of leukocyte chemotaxis. Physiol Rev. 78:949–967. 1998.PubMed/NCBI
14	Parekh AB and Putney JW Jr: Store-operated calcium channels. Physiol Rev. 85:757–810. 2005. View Article : Google Scholar : PubMed/NCBI
15	Lewis RS: The molecular choreography of a store-operated calcium channel. Nature. 446:284–287. 2007. View Article : Google Scholar : PubMed/NCBI
16	Salmon MD and Ahluwalia J: Pharmacology of receptor operated calcium entry in human neutrophils. Int Immunopharmacol. 11:145–148. 2011. View Article : Google Scholar : PubMed/NCBI
17	Feske S, Gwack Y, Prakriya M, et al: A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature. 441:179–185. 2006. View Article : Google Scholar : PubMed/NCBI
18	Roos J, DiGregorio PJ, Yeromin AV, et al: STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol. 169:435–445. 2005.PubMed/NCBI
19	Vig M, Peinelt C, Beck A, et al: CRACM1 is a plasma membrane protein essential for store-operated Ca²⁺ entry. Science. 312:1220–1223. 2006. View Article : Google Scholar : PubMed/NCBI
20	Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A and Hogan PG: Orai1 is an essential pore subunit of the CRAC channel. Nature. 443:230–233. 2006. View Article : Google Scholar : PubMed/NCBI
21	Yeromin AV, Zhang SL, Jiang W, Yu Y, Safrina O and Cahalan MD: Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature. 443:226–229. 2006. View Article : Google Scholar : PubMed/NCBI
22	Mercer JC, Dehaven WI, Smyth JT, et al: Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1. J Biol Chem. 281:24979–24990. 2006. View Article : Google Scholar : PubMed/NCBI
23	Peinelt C, Vig M, Koomoa DL, et al: Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat Cell Biol. 8:771–773. 2006. View Article : Google Scholar : PubMed/NCBI
24	Soboloff J, Spassova MA, Tang XD, Hewavitharana T, Xu W and Gill DL: Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem. 281:20661–20665. 2006. View Article : Google Scholar : PubMed/NCBI
25	Dolmetsch RE, Xu K and Lewis RS: Calcium oscillations increase the efficiency and specificity of gene expression. Nature. 392:933–936. 1998. View Article : Google Scholar : PubMed/NCBI
26	Lewis RS: Calcium signaling mechanisms in T lymphocytes. Annu Rev Immunol. 19:497–521. 2001. View Article : Google Scholar : PubMed/NCBI
27	Yoo AS, Cheng I, Chung S, et al: Presenilin-mediated modulation of capacitative calcium entry. Neuron. 27:561–572. 2000. View Article : Google Scholar : PubMed/NCBI
28	Parekh AB and Penner R: Store depletion and calcium influx. Physiol Rev. 77:901–930. 1997.PubMed/NCBI
29	Yang S, Zhang JJ and Huang XY: Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell. 15:124–134. 2009. View Article : Google Scholar : PubMed/NCBI
30	Schaff UY, Dixit N, Procyk E, Yamayoshi I, Tse T and Simon SI: Orai1 regulates intracellular calcium, arrest, and shape polarization during neutrophil recruitment in shear flow. Blood. 115:657–666. 2010. View Article : Google Scholar : PubMed/NCBI
31	Zou W, Meng X, Cai C, et al: Store-operated Ca²⁺ entry (SOCE) plays a role in the polarization of neutrophil-like HL-60 cells by regulating the activation of Akt, Src, and Rho family GTPases. Cell Physiol Biochem. 30:221–237. 2012.
32	Hauert AB, Martinelli S, Marone C and Niggli V: Differentiated HL-60 cells are a valid model system for the analysis of human neutrophil migration and chemotaxis. Int J Biochem Cell Biol. 34:838–854. 2002. View Article : Google Scholar : PubMed/NCBI
33	Li Z, Lu J, Xu P, Xie X, Chen L and Xu T: Mapping the interacting domains of STIM1 and Orai1 in Ca2+ release-activated Ca2+ channel activation. J Biol Chem. 282:29448–29456. 2007.PubMed/NCBI
34	Ji W, Xu P, Li Z, et al: Functional stoichiometry of the unitary calcium-release-activated calcium channel. Proc Natl Acad Sci USA. 105:13668–13673. 2008. View Article : Google Scholar : PubMed/NCBI
35	Zigmond SH: Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J Cell Biol. 75:606–616. 1977. View Article : Google Scholar
36	Heit B, Liu L, Colarusso P, Puri KD and Kubes P: PI3K accelerates, but is not required for, neutrophil chemotaxis to fMLP. J Cell Sci. 121:205–214. 2008. View Article : Google Scholar : PubMed/NCBI
37	Zou W, Chu X, Cai C, et al: AKT-mediated regulation of polarization in differentiated human neutrophil-like HL-60 cells. Inflamm Res. 61:853–862. 2012. View Article : Google Scholar : PubMed/NCBI
38	Cai C, Tang S, Wang X, et al: Requirement for both receptor-operated and store-operated calcium entry in N-formyl-methionine-leucine-phenylalanine-induced neutrophil polarization. Biochem Biophys Res Commun. 430:816–821. 2013. View Article : Google Scholar
39	Klokker M, Kharazmi A, Galbo H, Bygbjerg I and Pedersen BK: Influence of in vivo hypobaric hypoxia on function of lymphocytes, neutrocytes, natural killer cells, and cytokines. J Appl Physiol. 74:1100–1106. 1993.PubMed/NCBI
40	Simms HH and D’Amico R: Regulation of whole blood polymorphonuclear leukocyte phagocytosis following hypoxemia and hypoxemia/reoxygenation. Shock. 1:10–18. 1994. View Article : Google Scholar
41	Lee C, Xu DZ, Feketeova E, et al: Store-operated calcium channel inhibition attenuates neutrophil function and postshock acute lung injury. J Trauma. 59:56–63. 2005. View Article : Google Scholar : PubMed/NCBI
42	Hauser CJ, Fekete Z, Livingston DH, Adams J, Garced M and Deitch EA: Major trauma enhances store-operated calcium influx in human neutrophils. J Trauma. 48:592–597. 2000. View Article : Google Scholar : PubMed/NCBI