Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer

Janowska‐Wieczorek, Anna; Wysoczynski, Marcin; Kijowski, J.; Marquez‐Curtis, Leah A.; Machalinski, Bogdan; Ratajczak, Janina; Ratajczak, Mariusz Z.

doi:10.1002/ijc.20657

Cited by 660 publications

(512 citation statements)

References 49 publications

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“…These data are consistent with the previous report demonstrating an increased MMP-mediated invasion of lung cancer cells after contact with PMPs. 12 In contrast to the cited report, we did not observe a consistent parallel increase in the secretion of MMP-9. This discrepancy can be attributed to the difference in the used cancer types.…”

Section: Discussioncontrasting

confidence: 99%

Platelet‐derived microparticles promote invasiveness of prostate cancer cells via upregulation of MMP‐2 production

Dashevsky

Varon

Brill

2009

Intl Journal of Cancer

122

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Prostate cancer commonly affects men in the Western world. A major factor of the life-threatening course of this disease is the high rate of metastasis, predominantly to bones. Circulating tumor cells encounter platelets and may activate them, resulting in a production of microparticles (MPs). MPs are small platelet fragments expressing membrane receptors as well as cytoplasmic constituents. Here, we report that prostate cancer cells, Clone-1 (Cl-1), preincubated with platelet-derived MPs (PMPs), demonstrate increased invasion through a gelatin-coated (a denatured form of collagen) membrane of the Boyden chamber system. This effect was accompanied by an increased secretion of metalloproteinase-2 (MMP-2) as demonstrated by a gelatin zymography. Application of MMP-2/9 inhibitor reversed the PMP-induced tumor cell invasion. PMPs were shown to adhere to Cl-1 cells, but direct contact between them may not be mandatory for MMP secretion because PMP lysate induced MMP-2 production by Cl-1 cells to the same extent as did intact PMPs. PMP-induced MMP-2 secretion was inhibited by neutralization of either PKC or total intracellular tyrosine phosphorylation, but was not affected by blocking major intraplatelet cytokines. Actinomycin D (a transcription inhibitor) did not modify this effect, whereas cycloheximide (an inhibitor of protein translation) abolished the MMP-2 release. MMP-2 secretion was accompanied by a rapid and transient increase in MMP-2 mRNA level after a 2-hr coincubation of prostate cancer cells with PMPs. Thus, PMPs promote tumor invasiveness, at least in part by stimulation of MMP-2 production. ' 2008 Wiley-Liss, Inc.Key words: platelet-derived microparticles; prostate cancer; MMP-2 Platelet involvement in dissemination of tumor metastasis was first experimentally demonstrated several decades ago. 1 Potential mechanisms of the platelet effect on metastatic dissemination include PAR receptors, platelet-derived lysophosphatidic acid and others. 2,3 Platelets were previously shown to directly mediate tumor cell adhesion to the vascular wall thus facilitating their future egress into tissues. 4 However, functional platelet depletion several weeks after tumor inoculation also results in reduction of metastasis, 3 an effect that cannot be explained by decreased tumor cell survival or extravasation. In addition, platelets may serve as a source of numerous proangiogenic cytokines that support growth of new capillaries in the vicinity of metastasis. 5 Angiogenesis is a prerequisite for tumor growth. 6 The ability of platelets as a cellular system to induce angiogenesis in spite of numerous antiangiogenic compounds in their alpha-granules has recently been demonstrated. 7,8 Matrix metalloproteinases (MMPs) belong to a family of zinccontaining enzymes that are tightly involved in the angiogenic process as well as in tumor cell extravasation and metastasis. 9 Among this group of endopeptidases, MMP-2 and MMP-9 are considered most important for metastatic spread. Both enzymes cleave collagen that constitutes a major co...

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Section: Discussioncontrasting

confidence: 99%

Platelet‐derived microparticles promote invasiveness of prostate cancer cells via upregulation of MMP‐2 production

Dashevsky

Varon

Brill

2009

Intl Journal of Cancer

122

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“…MVs, SDF-1 and soluble CD40 ligand exhibited the same changes (days 0 vs 5: MVs, respectively, 219 ± 35 vs 492 ± 53/ml, Po0.01; SDF-1, 1.219±271 vs 1.789±430 pg/ml, Po0.05; soluble CD40 ligand, 1.8 ± 0.4 vs 4.1 ± 0.6 ng/ml, Po0.01; Figure 1). Janowska-Wieczorek et al 8 suggested that MVs actively released from cells may have an important role in cellto-cell communication. The reports by Deregibus et al 6 and Ratajczak et al 9 have developed this view.…”

mentioning

confidence: 99%

α4-integrin-positive microvesicles and SDF-1 in peripheral blood stem cell harvest

Nomura

Ishii

Inami

et al. 2008

Bone Marrow Transplant

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“…We assessed the presence of CXCR4 + microparticles in the peripheral blood and bone marrow samples by a combination of three different approaches (i.e., flow cytometry, ELISA, and Western blot analyses). In flow cytometry, we used CXCR4 + microparticles at an equal dose of 30 Ag protein/mL that was applied previously in various functional tests (22,28). As depicted in Fig.…”

Section: Resultsmentioning

confidence: 99%

“…They are able to transfer various receptors, including CXCR4, to the membranes of target cells, thus triggering a variety of biological responses, such as proliferation, survival, adhesion, chemotaxis, and engraftment of hematopoietic stem/progenitor cells (reviewed by ref. 21), as well as inducing metastasis and angiogenesis in lung (22) and breast cancer (23). Along with megakaryocyte-derived microparticles, they can also transfer CXCR4 to CXCR4-null cells, rendering them susceptible to HIV (24).…”

Section: Introductionmentioning

confidence: 99%

Functional CXCR4-Expressing Microparticles and SDF-1 Correlate with Circulating Acute Myelogenous Leukemia Cells

et al. 2006

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Stromal cell-derived factor-1 (SDF-1/CXCL12) and its receptor CXCR4 are implicated in the pathogenesis and prognosis of acute myelogenous leukemia (AML). Cellular microparticles, submicron vesicles shed from the plasma membrane of various cells, are also associated with human pathology. In the present study, we investigated the putative relationships between the SDF-1/CXCR4 axis and microparticles in AML. We detected CXCR4-expressing microparticles (CXCR4 + microparticles) in the peripheral blood and bone marrow plasma samples of normal donors and newly diagnosed adult AML patients. In samples from AML patients, levels of CXCR4 + microparticles and total SDF-1 were elevated compared with normal individuals. The majority of CXCR4 + microparticles in AML patients were CD45 + , whereas in normal individuals, they were mostly CD41 + . Importantly, we found a strong correlation between the levels of CXCR4 + microparticle and WBC count in the peripheral blood and bone marrow plasma obtained from the AML patients. Of interest, levels of functional, noncleaved SDF-1 were reduced in these patients compared with normal individuals and also strongly correlated with the WBC count. Furthermore, our data indicate NH 2 -terminal truncation of the CXCR4 molecule in the microparticles of AML patients. However, such microparticles were capable of transferring the CXCR4 molecule to AML-derived HL-60 cells, enhancing their migration to SDF-1 in vitro and increasing their homing to the bone marrow of irradiated NOD/SCID/B2m null mice. The CXCR4 antagonist AMD3100 reduced these effects. Our findings suggest that functional CXCR4 + microparticles and SDF-1 are involved in the progression of AML. We propose that their levels are potentially valuable as an additional

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Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer

Abstract: The role of platelets in tumor progression and metastasis has been recognized but the mechanism of their action remains unclear.

Cited by 660 publications

References 49 publications

Platelet‐derived microparticles promote invasiveness of prostate cancer cells via upregulation of MMP‐2 production

Platelet‐derived microparticles promote invasiveness of prostate cancer cells via upregulation of MMP‐2 production

α4-integrin-positive microvesicles and SDF-1 in peripheral blood stem cell harvest

Functional CXCR4-Expressing Microparticles and SDF-1 Correlate with Circulating Acute Myelogenous Leukemia Cells

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