Skip to main content
Log in

Extracellular stress stimuli alter galectin expression profiles and adhesion characteristics of HL-60 cells

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Galectins, a family of soluble β-galactoside-binding proteins, are involved in the regulation of various cellular functions, which are essential for adaptive cellular stress responses (CSRs). Although expression patterns of galectins and galectin-binding glycans change during tissue development and cancer, the requirement and role of galectin networks in the CSRs are not completely understood. In this study, we report that the treatment of human promyelocytic HL-60 cells with stimuli mimicking hypoxia (CoCl2), inducing the endoplasmic reticulum stress (tunicamycin), and stimulating cell differentiation, result in stress-specific differential expression of galectin transcripts. In addition, we show that CoCl2 increases the expression of cell surface glycans recognized by both β-galactoside- and GlcNAc-binding lectins. Thus, microenvironmental stress changes the glycobiological status of cells representing expression profiles of endogenous lectins and corresponding glycans. These findings introduce a novel classification of galectins in HL-60 cells, which suggests diverse functions of galectin members in CSRs.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

References

  1. Bailey KM, Wojtkowiak JW, Hashim AI, Gillies RJ (2012) Targeting the metabolic microenvironment of tumors. Adv Pharmacol 65:63–107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Ackerman D, Simon MC (2014) Hypoxia, lipids, and cancer: surviving the harsh tumor microenvironment. Trends Cell Biol 24:472–478

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Simmons SO, Fan CY, Ramabhadran R (2009) Cellular stress response pathway system as a sentinel ensemble in toxicological screening. Toxicol Sci 111:202–225

    Article  CAS  PubMed  Google Scholar 

  4. Fulda S, Gorman AM, Hori O, Samali A (2010) Cellular stress responses: cell survival and cell death. Int J Cell Biol 2010:214074. doi:10.1155/2010/214074

    PubMed Central  PubMed  Google Scholar 

  5. Gabius HJ (ed) (2009) The sugar code: fundamentals of glycosciences. Wiley, Weinheim

    Google Scholar 

  6. Timoshenko AV (2015) Towards molecular mechanisms regulating the expression of galectins in cancer cells under microenvironmental stress conditions. Cell Mol Life Sci 72:4327–4340

    Article  CAS  PubMed  Google Scholar 

  7. Shamova EV, Gorudko IV, Drozd ES, Chizhik SA, Martinovich GG, Cherenkevich SN, Timoshenko AV (2011) Redox regulation of morphology, cell stiffness, and lectin-induced aggregation of human platelets. Eur Biophys J 40:195–208

    Article  CAS  PubMed  Google Scholar 

  8. Gorudko IV, Mukhortava AV, Caraher B, Ren M, Cherenkevich SN, Kelly GM, Timoshenko AV (2011) Lectin-induced activation of plasma membrane NADPH oxidase in cholesterol-depleted human neutrophils. Arch Biochem Biophys 516:173–181

    Article  CAS  PubMed  Google Scholar 

  9. Lahm H, André S, Hoeflich A, Fischer JR, Sordat B, Kaltner H, Wolf E, Gabius HJ (2001) Comprehensive galectin fingerprinting in a panel of 61 human tumor cell lines by RT-PCR and its implications for diagnostic and therapeutic procedures. J Cancer Res Clin Oncol 127:375–386

    Article  CAS  PubMed  Google Scholar 

  10. Thijssen VL, Heusschen R, Caers J, Griffioen AW (2015) Galectin expression in cancer diagnosis and prognosis: a systematic review. Biochim Biophys Acta 1855:235–247

    Google Scholar 

  11. Than NG, Romero R, Xu Y, Erez O, Xu Z, Bhatti G, Leavitt R, Chung TH, El-Azzamy H, LaJeunesse C, Wang B, Balogh A, Szalai G, Land S, Dong Z, Hassan SS, Chaiworapongsa T, Krispin TM, Kim CJ, Tarca AL, Papp Z, Bohn H (2014) Evolutionary origins of the placental expression of chromosome 19 cluster galectins and their complex dysregulation in preeclampsia. Placenta 35:855–865

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Abedin MJ, Kashio Y, Seki M, Nakamura K, Hirashima M (2003) Potential roles of galectins in myeloid differentiation into three different lineages. J Leukoc Biol 73:650–656

    Article  CAS  PubMed  Google Scholar 

  13. Le QT, Shi G, Cao H, Nelson DW, Wang Y, Chen EY, Zhao S, Kong C, Richardson D, O’Byrne KJ, Giaccia AJ, Koong AC (2005) Galectin-1: a link between tumor hypoxia and tumor immune privilege. J Clin Oncol 23:8932–8941

    Article  CAS  PubMed  Google Scholar 

  14. Ikemori RY, Machado CM, Furuzawa KM, Nonogaki S, Osinaga E, Umezawa K, de Carvalho MA, Verinaud L, Chammas R (2014) Galectin-3 up-regulation in hypoxic and nutrient deprived microenvironments promotes cell survival. PLoS ONE 9:e111592. doi:10.1371/journal.pone.0111592

    Article  PubMed Central  PubMed  Google Scholar 

  15. Wu D, Yotnda P (2011) Induction and testing of hypoxia in cell culture. J Vis Exp 54:e2899. doi:10.3791/2899

    Google Scholar 

  16. Cawley K, Deegan S, Samali A, Gupta S (2011) Assays for detecting the unfolded protein response. Methods Enzymol 490:31–51

    Article  CAS  PubMed  Google Scholar 

  17. Thijssen VL, Hulsmans S, Griffioen AW (2008) The galectin profile of the endothelium: altered expression and localization in activated and tumor endothelial cells. Am J Pathol 172:545–553

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Yang RY, Hsu DK, Yu L, Ni J, Liu FT (2001) Cell cycle regulation by galectin-12, a new member of the galectin superfamily. J Biol Chem 276:20252–20260

    Article  CAS  PubMed  Google Scholar 

  19. Humphries MJ (1998) Cell-substrate adhesion assay. In: Bonifacio JC et al (eds) Current protocols in cell biology. Wiley, New York, pp 9.1.1–9.1.11

    Google Scholar 

  20. Timoshenko AV, Kaltner H, André S, Gabius HJ, Lala PK (2010) Differential stimulation of VEGF-C production by adhesion/growth-regulatory galectins and plant lectins in human breast cancer cells. Anticancer Res 30:4829–4834

    CAS  PubMed  Google Scholar 

  21. Holcik M, Sonenberg N (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6:318–327

    Article  CAS  PubMed  Google Scholar 

  22. Zeng Y, Danielson KG, Albert TJ, Shapiro IM, Risbud MV (2007) HIF-1α is a regulator of galectin-3 expression in the intervertebral dics. J Bone Miner Res 22:1851–1861

    Article  CAS  PubMed  Google Scholar 

  23. Mujcic H, Hill RP, Koritzinsky M, Wouters BG (2014) Hypoxia signaling and the metastatic phenotype. Curr Mol Med 14:565–579

    Article  CAS  PubMed  Google Scholar 

  24. Jiang H, Zou J, Zhang H, Fu W, Zeng T, Huang H, Zhou F, Hou J (2015) Unfolded protein response inducers tunicamycin and dithiothreitol promote myeloma cell differentiation mediated by XBP-1. Clin Exp Med 15:85–96

    Article  CAS  PubMed  Google Scholar 

  25. Le Marer N (2000) Galectin-3 expression in differentiating human myeloid cells. Cell Biol Int 24:245–251

    Article  PubMed  Google Scholar 

  26. Ogino T, Ozaki M, Matsukawa A (2010) Oxidative stress enhances granulocytic differentiation in HL 60 cells, an acute promyelocytic leukemia cell line. Free Radic Res 44:1328–1337

    Article  CAS  PubMed  Google Scholar 

  27. Yamaoka A, Kuwubara I, Frigeri LG, Liu FT (1995) A human galectin-3 (εbp/Mac-2), stimulates superoxide production by neutrophils. J Immunol 154:3479–3487

    CAS  PubMed  Google Scholar 

  28. Dyer KD, Rosenberg HF (2001) Transcriptional regulation of galectin-10 (eosinophil Charcot-Leyden crystal protein): a GC box (−44 to −50) controls butyric acid induction of gene expression. Life Sci 69:201–212

    Article  CAS  PubMed  Google Scholar 

  29. Song X, Mohr AM, Rameshwar P, Anjaria D, Fekete Z, Hauser CJ, Livingston DH (2002) Delayed differentiation of HL-60 cells following exposure to hypoxia. J Surg Res 108:243–249

    Article  CAS  PubMed  Google Scholar 

  30. Heusschen R, Schulkens IA, van Beijnum J, Griffioen AW, Thijssen VL (2014) Endothelial LGALS9 splice variant expression in endothelial cell biology and angiogenesis. Biochim Biophys Acta 1842:284–292

    Article  CAS  PubMed  Google Scholar 

  31. Zhang F, Zheng M, Qu Y, Li J, Ji I, Feng B, Lu A, Li J, Wang M, Liu B (2009) Different roles of galectin-9 isoforms in modulating E-selectin expression and adhesion function in LoVo colon carcinoma cells. Mol Biol Rep 36:823–830

    Article  CAS  PubMed  Google Scholar 

  32. Biamonti G, Caceres JF (2009) Cellular stress and RNA splicing. Trends Biochem Sci 34:146–153

    Article  CAS  PubMed  Google Scholar 

  33. Le Mercier M, Mathieu V, Haibe-Kains B, Bontempi G, Mijatovic T, Decaestecker C, Kiss R, Lefranc F (2008) Knocking down galectin 1 in human hs683 glioblastoma cells impairs both angiogenesis and endoplasmic reticulum stress responses. J Neuropathol Exp Neurol 67:456–469

    Article  PubMed  Google Scholar 

  34. Guardia CM, Gauto DF, Di Lella S, Rabinovich GA, Martí MA, Estrin DA (2011) An integrated computational analysis of the structure, dynamics, and ligand binding interactions of the human galectin network. J Chem Inf Model 51:1918–1930

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Western Strategic Support for NSERC Success Seed Grant and UWO Internal Funds (Western University, London, Ontario). We also gratefully acknowledge C. Wong and M. Sharkh for their excellent technical assistance with several aspects of laboratory work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. V. Timoshenko.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 668 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Timoshenko, A.V., Lanteigne, J. & Kozak, K. Extracellular stress stimuli alter galectin expression profiles and adhesion characteristics of HL-60 cells. Mol Cell Biochem 413, 137–143 (2016). https://doi.org/10.1007/s11010-015-2647-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-015-2647-0

Keywords

Navigation