Detection of erythroid progenitors and erythrocytopathies in patients with severe COVID-19 disease

Mamdouh A. Allahyani; Abdulelah A. Aljuaid; Mazen M. Almehmadi; Ahmad A. Alghamdi; Ibrahim F. Halawani; Abdullah F. Aldairi; Ahmad M. Alharbi; Mohammad H. Albshri; Abdulqader A. Mutwalli; Ayman S. Alhazmi

doi:10.15537/smj.2022.43.8.20220311

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Characteristics of peripheral lymphocyte subset alteration in COVID-19 pneumonia. J Infect Dis 2020; 221: 1762–1769.
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Dynamic changes in lymphocyte subsets and parallel cytokine levels in patients with severe and critical COVID-19. BMC Infect Dis 2021; 21: 79.
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2. Christopher D,
3. Tan GB,
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Peripheral lymphocyte subset alterations in COVID-19 patients. Int J Lab Hematol 2020; 42: 199–203.
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1. Yang G,
2. Feng F,
3. Li X,
4. Zhang T,
5. Li X,
6. Li B
. Changes of lymphocyte subsets in patients with COVID-19 and clinical significance: a case-control observational study. J Bio-X Res 2021; 4: 36–39.
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1. Jesenak M,
2. Brndiarova M,
3. Urbancikova I,
4. Rennerova Z,
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6. Bobcakova A, et al.
Immune parameters and COVID-19 infection – associations with clinical severity and disease prognosis. Front Cell Infect Microbiol 202; 10: 364.
6.↵
1. Thomas T,
2. Stefanoni D,
3. Dzieciatkowska M,
4. Issaian A,
5. Nemkov T,
6. Hill RC, et al.
Evidence of structural protein damage and membrane lipid remodeling in red blood cells from COVID-19 patients. J Proteome Res 2020; 19: 4455–4469.
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7.↵
1. SShahbaz S,
2. Xu L,
3. Osman M,
4. Sligl W,
5. Shields J,
6. Joyce M, et al.
Erythroid precursors and progenitors suppress adaptive immunity and get invaded by SARS-CoV-2. Stem Cell Reports 2021; 16: 1165–1181.
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8.↵
1. Khawaja UA,
2. Shamsoddin E,
3. Desideri LF,
4. Tovani-Palone MR
. Infection of red blood cells by SARS-CoV-2: new evidence. Einstein (São Paulo) 2021; 19: eCE6285.
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9.↵
1. Balzanelli MG,
2. Distratis P,
3. Dipalma G,
4. Vimercati L,
5. Inchingolo AD,
6. Lazzaro R, et al.
Sars-CoV-2 Virus Infection May Interfere CD34+ Hematopoietic Stem Cells and Megakaryocyte–Erythroid Progenitors Differentiation Contributing to Platelet Defection towards Insurgence of Thrombocytopenia and Thrombophilia. Microorganisms 2021; 9: 1632.
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10.↵
1. Murphy P,
2. Glavey S,
3. Quinn J
. Anemia and red blood cell abnormalities in COVID-19. Leuk Lymphoma 2021; 62: 1539–1539.
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11.↵
1. Kubánková M,
2. Hohberger B,
3. Hoffmanns J,
4. Fürst J,
5. Herrmann M,
6. Guck J, et al.
Physical phenotype of blood cells is altered in COVID-19. Biophys J 2021; 120: 2838–2847.
OpenUrl
12.↵
1. Bapat A,
2. Schippel N,
3. Shi X,
4. Jasbi P,
5. Gu H,
6. Kala M, et al.
Hypoxia promotes erythroid differentiation through the development of progenitors and proerythroblasts. Exp Hematol 2021; 97: 32–46.
OpenUrl
13.↵
1. Bernardes JP,
2. Mishra N,
3. Tran F,
4. Bahmer T,
5. Best L,
6. Blase JI, et al.
Longitudinal multi-omics analyses identify responses of megakaryocytes, erythroid cells, and plasmablasts as hallmarks of severe COVID-19. Immunity 2020; 53: 1296–1314.
OpenUrl
14.↵
1. Encabo HH,
2. Grey W,
3. Garcia-albornoz M,
4. Wood H,
5. Ulferts R,
6. Aramburu IV, et al.
Human erythroid progenitors are directly infected by SARS-CoV-2: implications for emerging erythropoiesis in severe COVID-19 patients. Stem Cell Reports 2021; 16: 428–436.
OpenUrl
15.↵
1. Aoki T
. A comprehensive review of our current understanding of red blood cell (RBC) glycoproteins. Membranes 2017; 7: 56.
OpenUrl
16.↵
1. Jaskiewicz E,
2. Jodłowska M,
3. Kaczmarek R,
4. Zerka A
. Erythrocyte glycophorins as receptors for Plasmodium merozoites. Parasit Vectors 2019; 12: 317.
OpenUrl
17.↵
1. Cosic I,
2. Cosic D,
3. Loncarevic I
. RRM prediction of erythrocyte band 3 protein as alternative receptor for SARS-CoV-2 Virus. Appl Sci 2020; 10: 4053.
OpenUrl
18.↵
1. Foy BH,
2. Carlson JCT,
3. Reinertsen E,
4. Padros I.
5. Valls R,
6. Pallares Lopez R,
7. Palanques-Tost E, et al.
Association of red blood cell distribution width with mortality risk in hospitalized adults with SARS-CoV-2 infection. JAMA Netw Open 2020; 3: e2022058.
OpenUrl
19.↵
1. Mello F V,
2. Land MGP,
3. Costa ES,
4. Teodósio C,
5. Sanchez ML,
6. Bárcena P, et al.
Maturation-associated gene expression profiles during normal human bone marrow erythropoiesis. Cell Death Discov 2019; 5: 69.
OpenUrl
20.↵
1. Pretini V,
2. Koenen MH,
3. Kaestner L,
4. Fens MHAM,
5. Schiffelers RM,
6. Bartels M, et al.
Red blood cells: chasing interactions. Front Physiol 2019; 10: 1–17.
OpenUrl CrossRef
21.↵
1. Petersen JEV,
2. Saelens JW,
3. Freedman E,
4. Turner L,
5. Lavstsen T,
6. Fairhurst RM, et al.
Sickle-trait hemoglobin reduces adhesion to both CD36 and EPCR by Plasmodium falciparum-infected erythrocytes. PLoS Pathog 2021; 17: e1009659.
OpenUrl
22.↵
1. Bergamaschi G,
2. Borrelli de Andreis F,
3. Aronico N,
4. Lenti MV,
5. Barteselli C,
6. Merli S, et al.
Anemia in patients with Covid-19: pathogenesis and clinical significance. Clin Exp Med 2021; 21: 239–246.
OpenUrl
23.↵
1. Hariyanto TI,
2. Kurniawan A
. Anemia is associated with severe coronavirus disease 2019 (COVID-19) infection. Transfus Apher Sci 2020; 59: 102926.
OpenUrl
24.↵
1. Kaur G,
2. Sandeep F,
3. Olayinka O,
4. Gupta G
. Morphologic changes in circulating blood cells of COVID-19 patients. Cureus 2021; 13: 6–13.
OpenUrl
25.↵
1. Gabr H,
2. Bastawy S
, Abdel_Aal AA, Khalil NM, Fateen M. Changes in peripheral blood cellular morphology as diagnostic markers for COVID19 infection. Int J Lab Hematol 2022; 44: 1–7.
OpenUrl
26.↵
1. Pezeshki A,
2. Vaezi A,
3. Nematollahi P
. Blood cell morphology and COVID-19 clinical course, severity, and outcome. J Hematop 2021; 14: 221–228.
OpenUrl
27.↵
1. Della Rocca DG,
2. Magnocavallo M,
3. Lavalle C,
4. Romero J,
5. Forleo GB,
6. Tarantino N, et al.
Evidence of systemic endothelial injury and microthrombosis in hospitalized COVID-19 patients at different stages of the disease. J Thromb Thrombolysis 2021; 51: 571–576.
OpenUrl

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Phenotypical evaluation of lymphocytes and monocytes in patients with type 2 diabetes mellitus in Saudi Arabia

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Keywords

[1] 1.↵
Wang F,
Nie J,
Wang H,
Zhao Q,
Xiong Y,
Deng L, et al.
Characteristics of peripheral lymphocyte subset alteration in COVID-19 pneumonia. J Infect Dis 2020; 221: 1762–1769.
OpenUrl PubMed

[2] Wang F,

[3] Nie J,

[4] Wang H,

[5] Zhao Q,

[6] Xiong Y,

[7] Deng L, et al.

[8] 2.↵
Liu Y,
Tan W,
Chen H,
Zhu Y,
Wan L,
Jiang K, et al.
Dynamic changes in lymphocyte subsets and parallel cytokine levels in patients with severe and critical COVID-19. BMC Infect Dis 2021; 21: 79.
OpenUrl

[9] Liu Y,

[10] Tan W,

[11] Chen H,

[12] Zhu Y,

[13] Wan L,

[14] Jiang K, et al.

[15] 3.↵
Chan SSW,
Christopher D,
Tan GB,
Chong VCL,
Fan BE,
Lin CY, et al.
Peripheral lymphocyte subset alterations in COVID-19 patients. Int J Lab Hematol 2020; 42: 199–203.
OpenUrl

[16] Chan SSW,

[17] Christopher D,

[18] Tan GB,

[19] Chong VCL,

[20] Fan BE,

[21] Lin CY, et al.

[22] 4.↵
Yang G,
Feng F,
Li X,
Zhang T,
Li X,
Li B
. Changes of lymphocyte subsets in patients with COVID-19 and clinical significance: a case-control observational study. J Bio-X Res 2021; 4: 36–39.
OpenUrl

[23] Yang G,

[24] Feng F,

[25] Li X,

[26] Zhang T,

[27] Li X,

[28] Li B

[29] 5.↵
Jesenak M,
Brndiarova M,
Urbancikova I,
Rennerova Z,
Vojtkova J,
Bobcakova A, et al.
Immune parameters and COVID-19 infection – associations with clinical severity and disease prognosis. Front Cell Infect Microbiol 202; 10: 364.

[30] Jesenak M,

[31] Brndiarova M,

[32] Urbancikova I,

[33] Rennerova Z,

[34] Vojtkova J,

[35] Bobcakova A, et al.

[36] 6.↵
Thomas T,
Stefanoni D,
Dzieciatkowska M,
Issaian A,
Nemkov T,
Hill RC, et al.
Evidence of structural protein damage and membrane lipid remodeling in red blood cells from COVID-19 patients. J Proteome Res 2020; 19: 4455–4469.
OpenUrl

[37] Thomas T,

[38] Stefanoni D,

[39] Dzieciatkowska M,

[40] Issaian A,

[41] Nemkov T,

[42] Hill RC, et al.

[43] 7.↵
SShahbaz S,
Xu L,
Osman M,
Sligl W,
Shields J,
Joyce M, et al.
Erythroid precursors and progenitors suppress adaptive immunity and get invaded by SARS-CoV-2. Stem Cell Reports 2021; 16: 1165–1181.
OpenUrl

[44] SShahbaz S,

[45] Xu L,

[46] Osman M,

[47] Sligl W,

[48] Shields J,

[49] Joyce M, et al.

[50] 8.↵
Khawaja UA,
Shamsoddin E,
Desideri LF,
Tovani-Palone MR
. Infection of red blood cells by SARS-CoV-2: new evidence. Einstein (São Paulo) 2021; 19: eCE6285.
OpenUrl

[51] Khawaja UA,

[52] Shamsoddin E,

[53] Desideri LF,

[54] Tovani-Palone MR

[55] 9.↵
Balzanelli MG,
Distratis P,
Dipalma G,
Vimercati L,
Inchingolo AD,
Lazzaro R, et al.
Sars-CoV-2 Virus Infection May Interfere CD34+ Hematopoietic Stem Cells and Megakaryocyte–Erythroid Progenitors Differentiation Contributing to Platelet Defection towards Insurgence of Thrombocytopenia and Thrombophilia. Microorganisms 2021; 9: 1632.
OpenUrl

[56] Balzanelli MG,

[57] Distratis P,

[58] Dipalma G,

[59] Vimercati L,

[60] Inchingolo AD,

[61] Lazzaro R, et al.

[62] 10.↵
Murphy P,
Glavey S,
Quinn J
. Anemia and red blood cell abnormalities in COVID-19. Leuk Lymphoma 2021; 62: 1539–1539.
OpenUrl

[63] Murphy P,

[64] Glavey S,

[65] Quinn J

[66] 11.↵
Kubánková M,
Hohberger B,
Hoffmanns J,
Fürst J,
Herrmann M,
Guck J, et al.
Physical phenotype of blood cells is altered in COVID-19. Biophys J 2021; 120: 2838–2847.
OpenUrl

[67] Kubánková M,

[68] Hohberger B,

[69] Hoffmanns J,

[70] Fürst J,

[71] Herrmann M,

[72] Guck J, et al.

[73] 12.↵
Bapat A,
Schippel N,
Shi X,
Jasbi P,
Gu H,
Kala M, et al.
Hypoxia promotes erythroid differentiation through the development of progenitors and proerythroblasts. Exp Hematol 2021; 97: 32–46.
OpenUrl

[74] Bapat A,

[75] Schippel N,

[76] Shi X,

[77] Jasbi P,

[78] Gu H,

[79] Kala M, et al.

[80] 13.↵
Bernardes JP,
Mishra N,
Tran F,
Bahmer T,
Best L,
Blase JI, et al.
Longitudinal multi-omics analyses identify responses of megakaryocytes, erythroid cells, and plasmablasts as hallmarks of severe COVID-19. Immunity 2020; 53: 1296–1314.
OpenUrl

[81] Bernardes JP,

[82] Mishra N,

[83] Tran F,

[84] Bahmer T,

[85] Best L,

[86] Blase JI, et al.

[87] 14.↵
Encabo HH,
Grey W,
Garcia-albornoz M,
Wood H,
Ulferts R,
Aramburu IV, et al.
Human erythroid progenitors are directly infected by SARS-CoV-2: implications for emerging erythropoiesis in severe COVID-19 patients. Stem Cell Reports 2021; 16: 428–436.
OpenUrl

[88] Encabo HH,

[89] Grey W,

[90] Garcia-albornoz M,

[91] Wood H,

[92] Ulferts R,

[93] Aramburu IV, et al.

[94] 15.↵
Aoki T
. A comprehensive review of our current understanding of red blood cell (RBC) glycoproteins. Membranes 2017; 7: 56.
OpenUrl

[95] Aoki T

[96] 16.↵
Jaskiewicz E,
Jodłowska M,
Kaczmarek R,
Zerka A
. Erythrocyte glycophorins as receptors for Plasmodium merozoites. Parasit Vectors 2019; 12: 317.
OpenUrl

[97] Jaskiewicz E,

[98] Jodłowska M,

[99] Kaczmarek R,

[100] Zerka A

[101] 17.↵
Cosic I,
Cosic D,
Loncarevic I
. RRM prediction of erythrocyte band 3 protein as alternative receptor for SARS-CoV-2 Virus. Appl Sci 2020; 10: 4053.
OpenUrl

[102] Cosic I,

[103] Cosic D,

[104] Loncarevic I

[105] 18.↵
Foy BH,
Carlson JCT,
Reinertsen E,
Padros I.
Valls R,
Pallares Lopez R,
Palanques-Tost E, et al.
Association of red blood cell distribution width with mortality risk in hospitalized adults with SARS-CoV-2 infection. JAMA Netw Open 2020; 3: e2022058.
OpenUrl

[106] Foy BH,

[107] Carlson JCT,

[108] Reinertsen E,

[109] Padros I.

[110] Valls R,

[111] Pallares Lopez R,

[112] Palanques-Tost E, et al.

[113] 19.↵
Mello F V,
Land MGP,
Costa ES,
Teodósio C,
Sanchez ML,
Bárcena P, et al.
Maturation-associated gene expression profiles during normal human bone marrow erythropoiesis. Cell Death Discov 2019; 5: 69.
OpenUrl

[114] Mello F V,

[115] Land MGP,

[116] Costa ES,

[117] Teodósio C,

[118] Sanchez ML,

[119] Bárcena P, et al.

[120] 20.↵
Pretini V,
Koenen MH,
Kaestner L,
Fens MHAM,
Schiffelers RM,
Bartels M, et al.
Red blood cells: chasing interactions. Front Physiol 2019; 10: 1–17.
OpenUrl CrossRef

[121] Pretini V,

[122] Koenen MH,

[123] Kaestner L,

[124] Fens MHAM,

[125] Schiffelers RM,

[126] Bartels M, et al.

[127] 21.↵
Petersen JEV,
Saelens JW,
Freedman E,
Turner L,
Lavstsen T,
Fairhurst RM, et al.
Sickle-trait hemoglobin reduces adhesion to both CD36 and EPCR by Plasmodium falciparum-infected erythrocytes. PLoS Pathog 2021; 17: e1009659.
OpenUrl

[128] Petersen JEV,

[129] Saelens JW,

[130] Freedman E,

[131] Turner L,

[132] Lavstsen T,

[133] Fairhurst RM, et al.

[134] 22.↵
Bergamaschi G,
Borrelli de Andreis F,
Aronico N,
Lenti MV,
Barteselli C,
Merli S, et al.
Anemia in patients with Covid-19: pathogenesis and clinical significance. Clin Exp Med 2021; 21: 239–246.
OpenUrl

[135] Bergamaschi G,

[136] Borrelli de Andreis F,

[137] Aronico N,

[138] Lenti MV,

[139] Barteselli C,

[140] Merli S, et al.

[141] 23.↵
Hariyanto TI,
Kurniawan A
. Anemia is associated with severe coronavirus disease 2019 (COVID-19) infection. Transfus Apher Sci 2020; 59: 102926.
OpenUrl

[142] Hariyanto TI,

[143] Kurniawan A

[144] 24.↵
Kaur G,
Sandeep F,
Olayinka O,
Gupta G
. Morphologic changes in circulating blood cells of COVID-19 patients. Cureus 2021; 13: 6–13.
OpenUrl

[145] Kaur G,

[146] Sandeep F,

[147] Olayinka O,

[148] Gupta G

[149] 25.↵
Gabr H,
Bastawy S
, Abdel_Aal AA, Khalil NM, Fateen M. Changes in peripheral blood cellular morphology as diagnostic markers for COVID19 infection. Int J Lab Hematol 2022; 44: 1–7.
OpenUrl

[150] Gabr H,

[151] Bastawy S

[152] 26.↵
Pezeshki A,
Vaezi A,
Nematollahi P
. Blood cell morphology and COVID-19 clinical course, severity, and outcome. J Hematop 2021; 14: 221–228.
OpenUrl

[153] Pezeshki A,

[154] Vaezi A,

[155] Nematollahi P

[156] 27.↵
Della Rocca DG,
Magnocavallo M,
Lavalle C,
Romero J,
Forleo GB,
Tarantino N, et al.
Evidence of systemic endothelial injury and microthrombosis in hospitalized COVID-19 patients at different stages of the disease. J Thromb Thrombolysis 2021; 51: 571–576.
OpenUrl

[157] Della Rocca DG,

[158] Magnocavallo M,

[159] Lavalle C,

[160] Romero J,

[161] Forleo GB,

[162] Tarantino N, et al.

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Detection of erythroid progenitors and erythrocytopathies in patients with severe COVID-19 disease

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Detection of erythroid progenitors and erythrocytopathies in patients with severe COVID-19 disease

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