Characterization of Phlebotomus papatasi Peritrophins, and the Role of PpPer1 in Leishmania major Survival in its Natural Vector
Publication Date
March 14, 2013
Journal
PLOS Neglected Tropical Diseases
Authors
Iliano V. Coutinho Abreu, Narinder K. Sharma, Maricela Robles Murguia & Marcelo Ramalho Ortigao
Volume
7
Issue
3
Pages
e2132
DOI
https://dx.plos.org/10.1371/journal.pntd.0002132
Publisher URL
http://journals.plos.org/plosntds/article?id=10.1371%2Fjournal.pntd.0002132
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23516661
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3597473
Europe PMC
http://europepmc.org/abstract/MED/23516661
Web of Science
000316943800045
Scopus
84876012132
Mendeley
http://www.mendeley.com/research/characterization-phlebotomus-papatasi-peritrophins-role-ppper1-leishmania-major-survival-natural-vec
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Mendeley | Further Information

{"title"=>"Characterization of Phlebotomus papatasi Peritrophins, and the Role of PpPer1 in Leishmania major Survival in its Natural Vector", "type"=>"journal", "authors"=>[{"first_name"=>"Iliano V.", "last_name"=>"Coutinho-Abreu", "scopus_author_id"=>"14019092300"}, {"first_name"=>"Narinder K.", "last_name"=>"Sharma", "scopus_author_id"=>"57199924851"}, {"first_name"=>"Maricela", "last_name"=>"Robles-Murguia", "scopus_author_id"=>"36705056100"}, {"first_name"=>"Marcelo", "last_name"=>"Ramalho-Ortigao", "scopus_author_id"=>"6506584708"}], "year"=>2013, "source"=>"PLoS Neglected Tropical Diseases", "identifiers"=>{"sgr"=>"84876012132", "doi"=>"10.1371/journal.pntd.0002132", "pui"=>"368694482", "pmid"=>"23516661", "scopus"=>"2-s2.0-84876012132", "issn"=>"19352735"}, "id"=>"389bc2cf-4ec6-3f0c-b30b-ca815c79272a", "abstract"=>"The peritrophic matrix (PM) plays a key role in compartmentalization of the blood meal and as barrier to pathogens in many disease vectors. To establish an infection in sand flies, Leishmania must escape from the endoperitrophic space to prevent excretion with remnants of the blood meal digestion. In spite of the role played regarding Leishmania survival, little is known about sand fly PM molecular components and structural organization. We characterized three peritrophins (PpPer1, PpPer2, and PpPer3) from Phlebotomus papatasi. PpPer1 and PpPer2 display, respectively, four and one chitin-binding domains (CBDs). PpPer3 on the other hand has two CBDs, one mucin-like domain, and a putative domain with hallmarks of a CBD, but with changes in key amino acids. Temporal and spatial expression analyses show that PpPer1 is expressed specifically in the female midgut after blood feeding. PpPer2 and PpPer3 mRNAs were constitutively expressed in midgut and hindgut, with PpPer3 also being expressed in Malpighian tubules. PpPer2 was the only gene expressed in developmental stages. Interestingly, PpPer1 and PpPer3 expression are regulated by Le. major infection. Recombinant PpPer1, PpPer2 and PpPer3 were obtained and shown to display similar biochemical profiles as the native; we also show that PpPer1 and PpPer2 are able to bind chitin. Knockdown of PpPer1 led to a 44% reduction in protein, which in spite of producing an effect on the percentage of infected sand flies, resulted in a 39% increase of parasite load at 48 h. Our data suggest that PpPer1 is a component for the P. papatasi PM and likely involved in the PM role as barrier against Le. major infection.", "link"=>"http://www.mendeley.com/research/characterization-phlebotomus-papatasi-peritrophins-role-ppper1-leishmania-major-survival-natural-vec", "reader_count"=>16, "reader_count_by_academic_status"=>{"Student > Doctoral Student"=>2, "Researcher"=>3, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Student > Doctoral Student"=>2, "Researcher"=>3, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>10, "Medicine and Dentistry"=>1, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/987772"], "description"=>"<p>Western blots were carried out with 6×His-tagged rPpPer1, rPpPer2, and rPpPer3 (250 ng each protein) obtained from FreeStyle CHO-S cells. Proteins were separated on 4–12% reducing NuPAGE gels. (<b>A</b>) Proteins were transferred to nitrocellulose and incubated with anti-His antibody (1∶2,000), followed by anti-mouse AP-conjugated (1∶10,000). Lanes: M, molecular weight marker; 1, PpPer1; 2, PpPer2; 3, PpPer3. (<b>B</b>) rPpPer2 (200 ng) was <i>N</i>-deglycosylated with 1,000 (lane 2), 2,000 (lane 3) and 3,000 (lane 4) units of PNGase F for 16 h at 37°C (untreated rPpPer2 control lane 1). Separated proteins were transferred to nitrocellulose and incubated with anti-His followed anti-mouse AP-conjugated. M: molecular weight marker. Arrows indicate the 16 kDa and 20-to-24 kDa bands seen on rPpPer2 preparations (<b>A</b> and <b>B</b>). After PNGase F treatment the 20-to-24 kDa bands are no longer detected.</p>", "links"=>[], "tags"=>["genetics and genomics"], "article_id"=>652429, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132.g006", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Recombinant_proteins_/652429", "title"=>"Recombinant proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-15 11:33:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/987768"], "description"=>"<p>qRT-PCR assays depicting differences in PpPer1 (<b>A</b>), PpPer2 (<b>B</b>), and PpPer3 (<b>C</b>) mRNA levels between non-infected and <i>Le. major</i> infected midguts dissected at 24 h, 48 h, and 72 h PBM. Each dot (symbol) represents the mRNA expression levels in a single midgut whereas horizontal bars indicate mean expression levels. The cDNA encoding the S3 protein of the 40S ribosomal subunit was used as the housekeeping control gene. The mean expression of non-infected midguts was used as a standard (100%) for comparisons to the percentage of mRNA expression of <i>Le. major</i> infected midguts for each time point. NI: Non-infected. INF: <i>Le. major</i> infected. NS: Not significant. *: Statistically significant, p<0.05.</p>", "links"=>[], "tags"=>["peritrophin", "mrna"], "article_id"=>652425, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132.g005", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Modulation_of_peritrophin_mRNA_expression_upon_Le_major_infection_/652425", "title"=>"Modulation of peritrophin mRNA expression upon <i>Le. major</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-15 11:33:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/987766"], "description"=>"<p>Expression of <i>PpPer1</i>, <i>PpPer2</i>, and <i>PpPer3</i> mRNAs was assessed by RT-PCR (23–25 cycles) in <i>P. papatasi</i> midguts dissected from adult females at different time points before and after blood feeding (0–144 hours PBM) (<b>A</b>); in pools of tissues other than midgut (<b>B</b>); and in eggs (pool of 20 eggs) or whole body of larvae and pupae (<b>C</b>). β-Tub was used as the housekeeping control gene. The size of the cDNA fragments amplified were 122 bp (<i>PpPer1</i>), 168 bp (<i>PpPer2</i>), 121 bp (<i>PpPer3</i>), and 148 bp (β-Tub). CC: Carcass. HG: Hindgut. FB: Fat Body. HS: Head along with salivary glands. OV: Ovaries. MT: Malpighian Tubules. E: Eggs. L1: Larval stage 1. L2: Larval stage 2. L3: Larval stage 3. L4: Larval stage 4. P: Pupa. (-): Negative control.</p>", "links"=>[], "tags"=>["mrna"], "article_id"=>652423, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132.g003", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Peritrophin_mRNA_expression_profiles_/652423", "title"=>"Peritrophin mRNA expression profiles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-15 11:32:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/987767"], "description"=>"<p>Expression of native PpPer1 and PpPer3 in <i>P. papatasi</i> midgut lysates was assessed using one midgut equivalent (from pools of five guts for each time point) of non blood fed and blood fed <i>P. papatasi</i> per lane. Lanes: M, size marker; 1, non blood fed midgut; 2, blood fed midgut dissected 24 h PBM; 3, blood fed midgut dissected 48 h PBM; 4, blood fed midgut dissected 72 h PBM; 5, blood fed midgut dissected 96 h PBM. Proteins were transferred to nitrocellulose and blots were incubated with anti-PpPer1 (A) and with anti-PpPer3 (B) specific antisera. Arrows point the native proteins PpPer1 (A) and PpPer3 (B).</p>", "links"=>[], "tags"=>["ppper1", "ppper3", "midgut"], "article_id"=>652424, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132.g004", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_PpPer1_and_PpPer3_in_P_papatasi_midgut_lysates_/652424", "title"=>"Expression of PpPer1 and PpPer3 in <i>P. papatasi</i> midgut lysates.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-15 11:32:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/987780"], "description"=>"<p>Knockdown of PpPer1 leads to greater <i>Le. major</i> load in the midgut of <i>P. papatasi</i>. At 48 h post-infection (<b>A</b>), dsPpPer1 (dsPer1) injection caused an increased (39%; p<0.05 Mann-Whitney U test) in <i>Le. major</i> load compared to dsGFP-injected <i>P. papatasi</i>. Results shown are from combined data of two independent experiments. (<b>B</b>) Although not statistically significant, <i>PpPer1</i> knockdown led to 22% increase in <i>Le. major</i> load in <i>P. papatasi</i> midguts at 96 h post-infection when compared to dsGFP-injected. Each dot (filled circle or square) represents number of <i>Le. major</i> in a single midgut whereas horizontal bars indicate mean parasite number. <i>P. papatasi</i> were infected with 5×10<sup>6 </sup><i>Le. major</i> amastigotes/ml in heat-inactivated mouse blood. N: Number of <i>P. papatasi</i> midguts dissected. NS: Not significant. *: Statistically significant, p<0.05.</p>", "links"=>[], "tags"=>["ppper1", "knockdown"], "article_id"=>652437, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132.g009", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_PpPer1_knockdown_on_Le_major_infection_/652437", "title"=>"Effects of PpPer1 knockdown on <i>Le. major</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-15 11:35:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/987762"], "description"=>"<p>Multiple sequence alignment was performed with individual CBD domains identified from peritrophins from <i>P. papatasi</i> and <i>L. longipalpis</i>. Pp1CBD1, Pp1CBD2, Pp1CBD3, and Pp1CBD4 are PpPer1 CBDs. Pp2CBD1 is the single CBD in PpPer2. Pp3CBD1 and Pp3CBD2 are the two CBDs identified in PpPer3. Lulo1CBD1, Lulo1CBD2, Lulo1CBD3, and Lulo1CBD4 are the four CBDs in LuloPer1. Lulo2CBD1 and Lulo3CBD1 are the single CBDs in LuloPer2 and in LuloPer3, respectively. Ll3CBD1 and Ll3CBD2 are CBDs in LlPer3. Pp3put and Ll3put are putative domains similar to CBDs identified in <i>P. papatasi</i> PpPer3 and in <i>L. longipalpis</i> Ll3Per3. Such putative domain sequences also were identified in the N-terminal region of <i>C. felis</i> PL1 - CfPl1put; <i>C. quinquefasciatus</i> conserved hypothetical protein - Cq16put; and <i>A. aegypti</i> Ae51put, Ae45put, and Ae52put. The six conserved cysteines are highlighted in grey with the conserved aromatic amino acids predicted to bind chitin shown in white with black highlight; HRM motifs are underlined. Conserved amino acid residues displayed exclusively by the putative CBD domain sequences are shown in red, and the additional cysteine residues are indicated by asterisk (*).</p>", "links"=>[], "tags"=>["genetics and genomics"], "article_id"=>652419, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132.g001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Multiple_sequence_alignment_/652419", "title"=>"Multiple sequence alignment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-15 11:31:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/1007200"], "description"=>"<p>Primer name, sequence, and annealing temperatures for the primer pairs used in dsRNA synthesis and real time PCR analyses.</p>*<p>Described in Materials and Methods.</p>", "links"=>[], "tags"=>["genetics and genomics"], "article_id"=>667828, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132.t001", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primers_list_/667828", "title"=>"Primers list.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-03-14 02:10:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/987774"], "description"=>"<p>Recombinant rPpPer1 and rPpPer2 were assayed for the capacity to bind colloidal chitin. Wash and elute fractions corresponding to PpPer1 (<b>A</b>) and rPpPer2 (<b>B</b>) were loaded onto reducing 4–12% NuPAGE gels. Lanes: M, molecular weight marker; 1, unbound fraction; 2, wash 1 (10 mM sodium phosphate buffer, pH 8.0); 3, wash 2 (10 mM sodium phosphate buffer, pH 8.0 - 1M sodium chloride); 4, wash 3 (0.1 M acetic acid); 5, elute (SDS lysis buffer); 6, purified protein. Proteins were transferred and blots were incubated with anti-His followed by anti-mouse AP-conjugated.</p>", "links"=>[], "tags"=>["binding"], "article_id"=>652431, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chitin_binding_assay_/652431", "title"=>"Chitin binding assay.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-15 11:34:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/987784"], "description"=>"<div><p>The peritrophic matrix (PM) plays a key role in compartmentalization of the blood meal and as barrier to pathogens in many disease vectors. To establish an infection in sand flies, <i>Leishmania</i> must escape from the endoperitrophic space to prevent excretion with remnants of the blood meal digestion. In spite of the role played regarding <i>Leishmania</i> survival, little is known about sand fly PM molecular components and structural organization. We characterized three peritrophins (PpPer1, PpPer2, and PpPer3) from <i>Phlebotomus papatasi</i>. PpPer1 and PpPer2 display, respectively, four and one chitin-binding domains (CBDs). PpPer3 on the other hand has two CBDs, one mucin-like domain, and a putative domain with hallmarks of a CBD, but with changes in key amino acids. Temporal and spatial expression analyses show that <i>PpPer1</i> is expressed specifically in the female midgut after blood feeding. <i>PpPer2</i> and <i>PpPer3</i> mRNAs were constitutively expressed in midgut and hindgut, with <i>PpPer3</i> also being expressed in Malpighian tubules. <i>PpPer2</i> was the only gene expressed in developmental stages. Interestingly, <i>PpPer1</i> and <i>PpPer3</i> expression are regulated by <i>Le. major</i> infection. Recombinant PpPer1, PpPer2 and PpPer3 were obtained and shown to display similar biochemical profiles as the native; we also show that PpPer1 and PpPer2 are able to bind chitin. Knockdown of <i>PpPer1</i> led to a 44% reduction in protein, which in spite of producing an effect on the percentage of infected sand flies, resulted in a 39% increase of parasite load at 48 h. Our data suggest that PpPer1 is a component for the <i>P. papatasi</i> PM and likely involved in the PM role as barrier against <i>Le. major</i> infection.</p> </div>", "links"=>[], "tags"=>["characterization", "ppper1", "vector"], "article_id"=>652441, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132", "stats"=>{"downloads"=>1, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Characterization_of_Phlebotomus_papatasi_Peritrophins_and_the_Role_of_PpPer1_in_Leishmania_major_Survival_in_its_Natural_Vector__/652441", "title"=>"Characterization of <em>Phlebotomus papatasi</em> Peritrophins, and the Role of PpPer1 in <em>Leishmania major</em> Survival in its Natural Vector", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-15 11:35:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/987764"], "description"=>"<p>Condensed tree depicts all the putative CBD domains in a single branch (blue shadow box), displaying strong bootstrap support (84%). All other branches are CBDs found in orthologs of sand fly peritrophins. Filled circles, filled triangles, and open square indicate sand fly, mosquito, and flea peritrophins, respectively.</p>", "links"=>[], "tags"=>["genetics and genomics"], "article_id"=>652421, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132.g002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_comparison_/652421", "title"=>"Phylogenetic comparison.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-15 11:32:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/987777"], "description"=>"<p>(<b>A</b>) real time qRT-PCR showing <i>PpPer1</i> mRNA level reduction in dsRNA-injected (dsPer1) <i>P. papatasi</i> compared to control injected (GFP dsRNA). Knockdown effects in <i>PpPer1</i> mRNA expression were assessed at 24 h and 48 h PBM that corresponded to 72 h and 96 h post dsRNA injection. Each symbol represents mRNA expression levels in a single midgut. Horizontal bars indicate mean expression levels. The S3 gene was used as the housekeeping control gene. The mean expression of <i>PpPer1</i> in dsGFP-injected flies was used as 100% standard. NS: Not significant. *: Statistically significant, p<0.05 (Unpaired t-test). (<b>B</b>) Western blot assay showing reduction in PpPer1 protein levels at 24 h PBM (72 h after dsRNA injection) in dsPer1-injected flies compared to dsGFP-injected (chemiluminescence development). Nine and a half micrograms of protein were loaded onto 10% NuPAGE gel. (<b>C</b>) Densitometry showing 44% reduction in the intensity of PpPer1 protein band obtained after chemiluminescence development compared to the PpPer1 band intensity of dsGFP-injected flies. For all <i>PpPer1</i> knockdown assays, 80 ng of dsRNA was injected intrathoracically into 3-to-5 day old <i>P. papatasi</i> females fed on 30% sucrose solution <i>ad libitum</i>.</p>", "links"=>[], "tags"=>["knockdown", "mrna"], "article_id"=>652434, "categories"=>["Genetics"], "users"=>["Iliano V. Coutinho-Abreu", "Narinder K. Sharma", "Maricela Robles-Murguia", "Marcelo Ramalho-Ortigão"], "doi"=>"https://dx.doi.org/10.1371/journal.pntd.0002132.g008", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PpPer1_knockdown_at_mRNA_and_protein_levels_/652434", "title"=>"<i>PpPer1</i> knockdown at mRNA and protein levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-15 11:34:36"}

PMC Usage Stats | Further Information

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Relative Metric

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